A Neural Decision Signal during Internal Sampling from Working Memory in Humans.

How humans transform sensory information into decisions that steer purposeful behavior is a central question in psychology and neuroscience that is traditionally investigated during the sampling of external environmental signals. The decision-making framework of gradual information sampling toward a decision has also been proposed to apply when sampling internal sensory evidence from working memory. However, neural evidence for this proposal remains scarce. Here we show (using scalp EEG in male and female human volunteers) that sampling internal visual representations from working memory elicits a scalp EEG potential associated with gradual evidence accumulation-the central parietal positivity. Consistent with an evolving decision process, we show how this signal (1) scales with the time participants require to reach a decision about the cued memory content and (2) is amplified when having to decide among multiple contents in working memory. These results bring the electrophysiology of decision-making into the domain of working memory and suggest that variability in memory-guided behavior may be driven (at least in part) by variations in the sampling of our inner mental contents.

Prospection of Potential Actions during Visual Working Memory Starts Early, Is Flexible, and Predicts Behavior.

For visual working memory to serve upcoming behavior, it is crucial that we prepare for the potential use of working-memory contents ahead of time. Recent studies have demonstrated how the prospection and planning for an upcoming manual action starts early after visual encoding, and occurs alongside visual retention. Here, we address whether such "output planning" in visual working memory flexibly adapts to different visual-motor mappings, and occurs even when an upcoming action will only potentially become relevant for behavior. Human participants (female and male) performed a visual-motor working memory task in which they remembered one or two colored oriented bars for later (potential) use. We linked, and counterbalanced, the tilt of the visual items to specific manual responses. This allowed us to track planning of upcoming behavior through contralateral attenuation of ß band activity, a canonical motor-cortical EEG signature of manual-action planning. The results revealed how action encoding and subsequent planning alongside visual working memory (1) reflect anticipated task demands rather than specific visual-motor mappings, (2) occur even for actions that will only potentially become relevant for behavior, and (3) are associated with faster performance for the encoded item, at the expense of performance to other working-memory content. This reveals how the potential prospective use of visual working memory content is flexibly planned early on, with consequences for the speed of memory-guided behavior.SIGNIFICANCE STATEMENT It is increasingly studied how visual working memory helps us to prepare for the future, in addition to how it helps us to hold onto the past. Recent studies have demonstrated that the planning of prospective actions occurs alongside encoding and retention in working memory. We show that such early "output planning" flexibly adapts to varying visual-motor mappings, occurs both for certain and potential actions, and predicts ensuing working-memory guided behavior. These results highlight the flexible and future-oriented nature of visual working memory, and provide insight into the neural basis of the anticipatory dynamics that translate visual representations into adaptive upcoming behavior.

Multiple and Dissociable Effects of Sensory History on Working-Memory Performance.

Behavioral reports of sensory information are biased by stimulus history. The nature and direction of such serial-dependence biases can differ between experimental settings; both attractive and repulsive biases toward previous stimuli have been observed. How and when these biases arise in the human brain remains largely unexplored. They could occur either via a change in sensory processing itself and/or during postperceptual processes such as maintenance or decision-making. To address this, we tested 20 participants (11 female) and analyzed behavioral and magnetoencephalographic (MEG) data from a working-memory task in which participants were sequentially presented with two randomly oriented gratings, one of which was cued for recall at the end of the trial. Behavioral responses showed evidence for two distinct biases: (1) a within-trial repulsive bias away from the previously encoded orientation on the same trial, and (2) a between-trial attractive bias toward the task-relevant orientation on the previous trial. Multivariate classification of stimulus orientation revealed that neural representations during stimulus encoding were biased away from the previous grating orientation, regardless of whether we considered the within-trial or between-trial prior orientation, despite opposite effects on behavior. These results suggest that repulsive biases occur at the level of sensory processing and can be overridden at postperceptual stages to result in attractive biases in behavior.SIGNIFICANCE STATEMENT Recent experience biases behavioral reports of sensory information, possibly capitalizing on the temporal regularity in our environment. It is still unclear at what stage of stimulus processing such serial biases arise. Here, we recorded behavior and neurophysiological [magnetoencephalographic (MEG)] data to test whether neural activity patterns during early sensory processing show the same biases seen in participants' reports. In a working-memory task that produced multiple biases in behavior, responses were biased toward previous targets, but away from more recent stimuli. Neural activity patterns were uniformly biased away from all previously relevant items. Our results contradict proposals that all serial biases arise at an early sensory processing stage. Instead, neural activity exhibited mostly adaptation-like responses to recent stimuli.

Neural Signatures of Competition between Voluntary and Involuntary Influences over the Focus of Attention in Visual Working Memory.

Adaptive behavior relies on the selection and prioritization of relevant sensory inputs from the external environment as well as from among internal sensory representations held in working memory. Recent behavioral evidence suggests that the classic distinction between voluntary (goal-driven) and involuntary (stimulus-driven) influences over attentional allocation also applies to the selection of internal representations held in working memory. In the current EEG study, we set out to investigate the neural dynamics associated with the competition between voluntary and involuntary control over the focus of attention in visual working memory. We show that when voluntary and involuntary factors compete for the internal focus of attention, prioritization of the appropriate item is delayed-as reflected both in delayed gaze biases that track internal selection and in delayed neural beta (15-25 Hz) dynamics that track the planning for the upcoming memory-guided manual action. We further show how this competition is paralleled-possibly resolved-by an increase in frontal midline theta (4-8 Hz) activity that, moreover, predicts the speed of ensuing memory-guided behavior. Finally, because theta increased following retrocues that effectively reduced working-memory load, our data unveil how frontal theta activity during internal attentional focusing tracks demands on cognitive control over and above working-memory load. Together, these data yield new insight into the neural dynamics that govern the focus of attention in visual working memory, and disentangle the contributions of frontal midline theta activity to the processes of control versus retention in working memory.

Turning Attention Inside Out: How Working Memory Serves Behavior.

Flexible behavior requires guidance not only by sensations that are available immediately but also by relevant mental contents carried forward through working memory. Therefore, selective-attention functions that modulate the contents of working memory to guide behavior (inside-out) are just as important as those operating on sensory signals to generate internal contents (outside-in). We review the burgeoning literature on selective attention in the inside-out direction and underscore its functional, flexible, and future-focused nature. We discuss in turn the purpose (why), targets (what), sources (when), and mechanisms (how) of selective attention inside working memory, using visual working memory as a model. We show how the study of internal selective attention brings new insights concerning the core cognitive processes of attention and working memory and how considering selective attention and working memory together paves the way for a rich and integrated understanding of how mind serves behavior.

Alpha oscillations track content-specific working memory capacity.

Though the neural basis of working memory (WM) capacity is often studied by exploiting inter-individual differences, capacity may also differ across memory materials within a given individual. Here, we exploit the content-dependence of WM capacity as a novel approach to investigate the oscillatory correlates of WM capacity, focusing on posterior 9-12 Hz alpha activity during retention. We recorded scalp electroencephalography (EEG) while male and female human participants performed WM tasks with varying memory loads (2 vs. 4 items) and materials (English letters vs. regular shapes vs. abstract shapes). First, behavioural data confirmed that memory capacity was fundamentally content-dependent: capacity for abstract shapes plateaued at around two, while the participants could remember more letters and regular shapes. Critically, content-specific capacity was paralleled in the degree of attenuation of EEG-alpha activity that plateaued in a similar, content-specific, manner. While we observed greater alpha attenuation for higher loads for all materials, we found larger load effects for letters and regular shapes than for abstract shapes - consistent with our behavioural data showing a lower capacity plateau for abstract shapes. Moreover, when only considering 2-item trials, alpha attenuation was greater for abstract shapes - where 2-items were close to the capacity plateau - than for other materials. Multivariate decoding of alpha-activity patterns reinforced these findings. Finally, for each material, load effects on capacity (K) and alpha attenuation were correlated across individuals. Our results demonstrate that alpha oscillations track memory capacity in a content-specific manner and track not just the number of items, but also their complexity.SIGNIFICANCE STATEMENTWorking memory (WM) is limited in its capacity. We show that capacity is not fixed for an individual but is rather memory-content dependent. Moreover, we used this as a novel approach to investigate the neural basis of WM capacity with EEG. We found that both behavioural capacity estimates and neural oscillations in the alpha band varied with memory loads and materials. The critical finding is a capacity plateau of approximately two items only for the more complex materials, accompanied by a similar plateau in the EEG alpha attenuation. The load effects on capacity and alpha attenuation were furthermore correlated across individuals for each of the materials. Our results demonstrate that alpha oscillations track the content-specific nature of WM capacity.

Heading Direction Tracks Internally Directed Selective Attention in Visual Working Memory.

We shift our gaze even when we orient attention internally to visual representations in working memory. Here, we show the bodily orienting response associated with internal selective attention is widespread as it also includes the head. In three virtual reality experiments, participants remembered 2 visual items. After a working memory delay, a central color cue indicated which item needed to be reproduced from memory. After the cue, head movements became biased in the direction of the memorized location of the cued memory item-despite there being no items to orient toward in the external environment. The heading-direction bias had a distinct temporal profile from the gaze bias. Our findings reveal that directing attention within the spatial layout of visual working memory bears a strong relation to the overt head orienting response we engage when directing attention to sensory information in the external environment. The heading-direction bias further demonstrates common neural circuitry is engaged during external and internal orienting of attention.

Anticipated moments: temporal structure in attention.

We have come to recognize the brain as a predictive organ, anticipating attributes of the incoming sensory stimulation to guide perception and action in the service of adaptive behaviour. In the quest to understand the neural bases of the modulatory prospective signals that prioritize and select relevant events during perception, one fundamental dimension has until recently been largely overlooked: time. In this Review, we introduce the burgeoning field of temporal attention and illustrate how the brain makes use of various forms of temporal regularities in the environment to guide adaptive behaviour and influence neural processing.

Goal-directed and stimulus-driven selection of internal representations.

Adaptive behavior relies on the selection of relevant sensory information from both the external environment and internal memory representations. In understanding external selection, a classic distinction is made between voluntary (goal-directed) and involuntary (stimulus-driven) guidance of attention. We have developed a task-the anti-retrocue task-to separate and examine voluntary and involuntary guidance of attention to internal representations in visual working memory. We show that both voluntary and involuntary factors influence memory performance but do so in distinct ways. Moreover, by tracking gaze biases linked to attentional focusing in memory, we provide direct evidence for an involuntary "retro-capture" effect whereby external stimuli involuntarily trigger the selection of feature-matching internal representations. We show that stimulus-driven and goal-directed influences compete for selection in memory, and that the balance of this competition-as reflected in oculomotor signatures of internal attention-predicts the quality of ensuing memory-guided behavior. Thus, goal-directed and stimulus-driven factors together determine the fate not only of perception, but also of internal representations in working memory.

Capacity and selection in immersive visual working memory following naturalistic object disappearance.

Visual working memory-holding past visual information in mind for upcoming behavior-is commonly studied following the abrupt removal of visual objects from static two-dimensional (2D) displays. In everyday life, visual objects do not typically vanish from the environment in front of us. Rather, visual objects tend to enter working memory following self or object motion: disappearing from view gradually and changing the spatial relation between memoranda and observer. Here, we used virtual reality (VR) to investigate whether two classic findings from visual working memory research-a capacity of around three objects and the reliance on space for object selection-generalize to more naturalistic modes of object disappearance. Our static reference condition mimicked traditional laboratory tasks whereby visual objects were held static in front of the participant and removed from view abruptly. In our critical flow condition, the same visual objects flowed by participants, disappearing from view gradually and behind the observer. We considered visual working memory performance and capacity, as well as space-based mnemonic selection, indexed by directional biases in gaze. Despite vastly distinct modes of object disappearance and altered spatial relations between memoranda and observer, we found comparable capacity and comparable gaze signatures of space-based mnemonic selection. This finding reveals how classic findings from visual working memory research generalize to immersive situations with more naturalistic modes of object disappearance and with dynamic spatial relations between memoranda and observer.

Rhythmic Modulation of Visual Perception by Continuous Rhythmic Auditory Stimulation.

At any given moment our sensory systems receive multiple, often rhythmic, inputs from the environment. Processing of temporally structured events in one sensory modality can guide both behavioral and neural processing of events in other sensory modalities, but whether this occurs remains unclear. Here, we used human electroencephalography (EEG) to test the cross-modal influences of a continuous auditory frequency-modulated (FM) sound on visual perception and visual cortical activity. We report systematic fluctuations in perceptual discrimination of brief visual stimuli in line with the phase of the FM-sound. We further show that this rhythmic modulation in visual perception is related to an accompanying rhythmic modulation of neural activity recorded over visual areas. Importantly, in our task, perceptual and neural visual modulations occurred without any abrupt and salient onsets in the energy of the auditory stimulation and without any rhythmic structure in the visual stimulus. As such, the results provide a critical validation for the existence and functional role of cross-modal entrainment and demonstrates its utility for organizing the perception of multisensory stimulation in the natural environment.SIGNIFICANCE STATEMENT Our sensory environment is filled with rhythmic structures that are often multi-sensory in nature. Here, we show that the alignment of neural activity to the phase of an auditory frequency-modulated (FM) sound has cross-modal consequences for vision: yielding systematic fluctuations in perceptual discrimination of brief visual stimuli that are mediated by accompanying rhythmic modulation of neural activity recorded over visual areas. These cross-modal effects on visual neural activity and perception occurred without any abrupt and salient onsets in the energy of the auditory stimulation and without any rhythmic structure in the visual stimulus. The current work shows that continuous auditory fluctuations in the natural environment can provide a pacing signal for neural activity and perception across the senses.

Planning the Potential Future during Multi-item Visual Working Memory.

Working memory allows us to retain visual information to guide upcoming future behavior. In line with this future-oriented purpose of working memory, recent studies have shown that action planning occurs during encoding and retention of a single visual item, for which the upcoming action is certain. We asked whether and how this extends to multi-item visual working memory, when visual representations serve the potential future. Human participants performed a visual working-memory task with a memory-load manipulation (one/two/four items) and a delayed orientation-reproduction report (of one item). We measured EEG to track 15- to 25-Hz beta activity in electrodes contralateral to the required response hand-a canonical marker of action planning. We show an attenuation of beta activity, not only in Load 1 (with one certain future action) but also in Load 2 (with two potential future actions), compared with Load 4 (with low prospective-action certainty). Moreover, in Load 2, potential action planning occurs regardless whether both visual items afford similar or dissimilar manual responses, and it predicts the speed of ensuing memory-guided behavior. This shows that potential action planning occurs during multi-item visual working memory and brings the perspective that working memory helps us prepare for the potential future.

10 Simple Rules for a Supportive Lab Environment.

The transition to principal investigator (PI), or lab leader, can be challenging, partially due to the need to fulfil new managerial and leadership responsibilities. One key aspect of this role, which is often not explicitly discussed, is creating a supportive lab environment. Here, we present ten simple rules to guide the new PI in the development of their own positive and thriving lab atmosphere. These rules were written and voted on collaboratively, by the students and mentees of Professor Mark Stokes, who inspired this piece.

Under the Mind's Hood: What We Have Learned by Watching the Brain at Work.

Imagine you were asked to investigate the workings of an engine, but to do so without ever opening the hood. Now imagine the engine fueled the human mind. This is the challenge faced by cognitive neuroscientists worldwide aiming to understand the neural bases of our psychological functions. Luckily, human ingenuity comes to the rescue. Around the same time as the Society for Neuroscience was being established in the 1960s, the first tools for measuring the human brain at work were becoming available. Noninvasive human brain imaging and neurophysiology have continued developing at a relentless pace ever since. In this 50 year anniversary, we reflect on how these methods have been changing our understanding of how brain supports mind.

Purpose-Dependent Consequences of Temporal Expectations Serving Perception and Action.

Temporal expectations enable anticipatory brain states that prepare us for upcoming perception and action. We investigated the purpose-dependent nature and consequences of cued temporal expectations on brain and behavior in male and female human volunteers, using two matched visual-motor tasks that stressed either response speed or visual accuracy. We show that the consequences of temporal expectations are fundamentally purpose dependent. Temporal expectations predominantly affected response times when visual demands were low and speed was more important, but perceptual accuracy when visual demands were more challenging. Using magnetoencephalography, we further show how temporal expectations latch onto anticipatory neural states associated with concurrent spatial expectations-modulating task-specific anticipatory neural lateralization of oscillatory brain activity in a modality- and frequency-specific manner. By relating these brain states to behavior, we finally reveal how the behavioral relevance of such anticipatory brain states is similarly purpose dependent.SIGNIFICANCE STATEMENT Knowing when events may occur helps to prepare neural activity for upcoming perception and action. It is becoming increasingly clear that distinct sources of temporal expectations may facilitate performance via distinct mechanisms. Another relevant dimension to consider regards the distinct purposes that temporal expectations may serve. Here, we demonstrate that the consequences of temporal expectations on neurophysiological brain activity and behavior are fundamentally purpose dependent, and show how temporal expectations interact with task-relevant neural states in a modality- and frequency-specific manner. This brings the important insight that the ways in which temporal expectations influence brain and behavior, and how brain activity is related to behavior, are not fixed properties but rather depend on the task at hand.

One Thing Leads to Another: Anticipating Visual Object Identity Based on Associative-Memory Templates.

Probabilistic associations between stimuli afford memory templates that guide perception through proactive anticipatory mechanisms. A great deal of work has examined the behavioral consequences and human electrophysiological substrates of anticipation following probabilistic memory cues that carry spatial or temporal information to guide perception. However, less is understood about the electrophysiological substrates linked to anticipating the sensory content of events based on recurring associations between successive events. Here, we demonstrate behavioral and electrophysiological signatures of using associative-memory templates to guide perception, while equating spatial and temporal anticipation (experiments 1 and 2), as well as target probability and response demands (experiment 2). By recording the electroencephalogram in the two experiments (N = 55; 24 females), we show that two markers in human electrophysiology implicated in spatial and temporal anticipation also contribute to the anticipation of perceptual identity, as follows: attenuation of alpha-band oscillations and the contingent negative variation (CNV). Together, our results show that memory-guided identity templates proactively impact perception and are associated with anticipatory states of attenuated alpha oscillations and the CNV. Furthermore, by isolating object-identity anticipation from spatial and temporal anticipation, our results suggest a role for alpha attenuation and the CNV in specific visual content anticipation beyond general changes in neural excitability or readiness.SIGNIFICANCE STATEMENT Probabilistic associations between stimuli afford memory templates that guide perception through proactive anticipatory mechanisms. The current work isolates the behavioral benefits and electrophysiological signatures of memory-guided identity-based anticipation, while equating anticipation of space, time, motor responses, and task relevance. Our results show that anticipation of the specific identity of a forthcoming percept impacts performance and is associated with states of attenuated alpha oscillations and the contingent negative variation, extending previous work implicating these neural substrates in spatial and temporal preparatory attention. Together, this work bridges fields of attention, memory, and perception, providing new insights into the neural mechanisms that support complex attentional templates.

Decoding visual colour from scalp electroencephalography measurements.

Recent advances have made it possible to decode various aspects of visually presented stimuli from patterns of scalp EEG measurements. As of recently, such multivariate methods have been commonly used to decode visual-spatial features such as location, orientation, or spatial frequency. In the current study, we show that it is also possible to track visual colour processing by using Linear Discriminant Analysis on patterns of EEG activity. Building on other recent demonstrations, we show that colour decoding: (1) reflects sensory qualities (as opposed to, for example, verbal labelling) with a prominent contribution from posterior electrodes contralateral to the stimulus, (2) conforms to a parametric coding space, (3) is possible in multi-item displays, and (4) is comparable in magnitude to the decoding of visual stimulus orientation. Through subsampling our data, we also provide an estimate of the approximate number of trials and participants required for robust decoding. Finally, we show that while colour decoding can be sensitive to subtle differences in luminance, our colour decoding results are primarily driven by measured colour differences between stimuli. Colour decoding opens a relevant new dimension in which to track visual processing using scalp EEG measurements, while bypassing potential confounds associated with decoding approaches that focus on spatial features.

Temporal Expectations Prepare Visual Working Memory for Behavior.

Working memory enables us to retain past sensations in service of anticipated task demands. How we prepare for anticipated task demands during working memory retention remains poorly understood. Here, we focused on the role of time-asking how temporal expectations help prepare for ensuing memory-guided behavior. We manipulated the expected probe time in a delayed change-detection task and report that temporal expectation can have a profound influence on memory-guided behavioral performance. EEG measurements corroborated the utilization of temporal expectations: demonstrating the involvement of a classic EEG signature of temporal expectation-the contingent negative variation-in the context of working memory. We also report the influence of temporal expectations on 2 EEG signatures associated with visual working memory-the lateralization of 8- to 12-Hz alpha activity, and the contralateral delay activity. We observed a dissociation between these signatures, whereby alpha lateralization (but not the contralateral delay activity) adapted to the time of expected memory utilization. These data show how temporal expectations prepare visual working memory for behavior and shed new light on the electrophysiological markers of both temporal expectation and working memory.

Comparing the prioritization of items and feature-dimensions in visual working memory.

Selective attention can be directed not only to external sensory inputs, but also to internal sensory representations held within visual working memory (VWM). To date, this phenomenon has been studied predominantly following retrospective cues directing attention to particular items, or their locations in memory. In addition to item-level attentional prioritization, recent studies have shown that selectively attending to feature dimensions in VWM can also improve memory recall performance. However, no study to date has directly compared item-based and dimension-based attention in VWM, nor their neural bases. Here, we compared the benefits of retrospective cues (retro-cues) that were directed either at a multifeature item or at a feature dimension that was shared between two spatially segregated items. Behavioral results revealed qualitatively similar attentional benefits in both recall accuracy and response time, but also showed that cueing benefits were larger after item cues. Concurrent electroencephalogram measurements further revealed a similar attenuation of posterior alpha oscillations following both item and dimension retro-cues when compared with noninformative, neutral retro-cues. We argue that attention can act flexibly to prioritize the most relevant information-at either the item or the dimension level-to optimize ensuing memory-based task performance, and we discuss the implications of the observed commonalities and differences between item-level and dimension-level prioritization in VWM.