A neural decision signal during internal sampling from working memory in humans.

How humans transform sensory information into decisions that steer purposeful behaviour 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 (CPP). Consistent with an evolving decision process, we show how this signal (i) scales with the time participants require to reach a decision about the cued memory content and (ii) 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 behaviour may be driven (at least in part) by variations in the sampling of our inner mental contents.Significance Statement A foundational question in the study of mind and brain is how we transform sensory information into decisions that steer adaptive behaviour. This is traditionally investigated during the sampling of external, environmental signals. Here, we demonstrate that a canonical EEG marker of decision making from the human perception literature - the CPP - also tracks gradual decision making when selecting and accessing internally stored visual information from working memory. These findings bridge the literatures on decision making and working memory and suggest that trial-to-trial variability in memory-guided behaviour is driven, at least in part, by variations in the sampling of our inner mental contents.

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.

Microsaccades Track Location-Based Object Rehearsal in Visual Working Memory.

Besides controlling eye movements, the brain's oculomotor system has been implicated in the control of covert spatial attention and the rehearsal of spatial information in working memory. We investigated whether the oculomotor system also contributes to rehearsing visual objects in working memory when object location is never asked about. To address this, we tracked the incidental use of locations for mnemonic rehearsal via directional biases in microsaccades while participants maintained two visual objects (colored oriented gratings) in working memory. By varying the stimulus configuration (horizontal, diagonal, and vertical) at encoding, we could quantify whether microsaccades were more aligned with the configurational axis of the memory contents, as opposed to the orthogonal axis. Experiment 1 revealed that microsaccades continued to be biased along the axis of the memory content several seconds into the working memory delay. In Experiment 2, we confirmed that this directional microsaccade bias was specific to memory demands, ruling out lingering effects from passive and attentive encoding of the same visual objects in the same configurations. Thus, by studying microsaccade directions, we uncover oculomotor-driven rehearsal of visual objects in working memory through their associated locations.

Shifting attention between perception and working memory.

Most everyday tasks require shifting the focus of attention between sensory signals in the external environment and internal contents in working memory. To date, shifts of attention have been investigated within each domain, but shifts between the external and internal domain remain poorly understood. We developed a combined perception and working-memory task to investigate and compare the consequences of shifting spatial attention within and between domains in the service of a common orientation-reproduction task. Participants were sequentially cued to attend to items either in working memory or to an upcoming sensory stimulation. Stay trials provided a baseline condition, while shift trials required participants to shift their attention to another item within the same or different domain. Validating our experimental approach, we found evidence that participants shifted attention effectively in either domain (Experiment 1). In addition, we observed greater costs when transitioning attention between as compared to within domains (Experiments 1, 2). Strikingly, these costs persisted even when participants were given more time to complete the attentional shift (Experiment 2). Biases in fixational gaze behaviour tracked attentional orienting in both domains, but revealed no latency or magnitude difference for within- versus between-domain shifts (Experiment 1). Collectively, the results from Experiments 1 and 2 suggest that shifting between attentional domains might be regulated by a unique control function. Our results break new ground for exploring the ubiquitous act of shifting attention between perception and working memory to guide adaptive behaviour in everyday cognition.

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.

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.

Attention in flux.

Selective attention comprises essential infrastructural functions supporting cognition-anticipating, prioritizing, selecting, routing, integrating, and preparing signals to guide adaptive behavior. Most studies have examined its consequences, systems, and mechanisms in a static way, but attention is at the confluence of multiple sources of flux. The world advances, we operate within it, our minds change, and all resulting signals progress through multiple pathways within the dynamic networks of our brains. Our aim in this review is to raise awareness of and interest in three important facets of how timing impacts our understanding of attention. These include the challenges posed to attention by the timing of neural processing and psychological functions, the opportunities conferred to attention by various temporal structures in the environment, and how tracking the time courses of neural and behavioral modulations with continuous measures yields surprising insights into the workings and principles of attention.

Microsaccades transiently lateralise EEG alpha activity.

The lateralisation of 8-12 Hz alpha activity is a canonical signature of human spatial cognition that is typically studied under strict fixation requirements. Yet, even during attempted fixation, the brain produces small involuntary eye movements known as microsaccades. Here we report how spontaneous microsaccades - made in the absence of incentives to look elsewhere - can themselves drive transient lateralisation of EEG alpha power according to microsaccade direction. This transient lateralisation of posterior alpha power occurs similarly following start and return microsaccades and is, at least for start microsaccades, driven by increased alpha power ipsilateral to microsaccade direction. This reveals new links between spontaneous microsaccades and human electrophysiological brain activity. It highlights how microsaccades are an important factor to consider in studies relating alpha activity - including spontaneous fluctuations in alpha activity - to spatial cognition, such as studies on visual attention, anticipation, and working memory.

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.

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.

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.

No obligatory trade-off between the use of space and time for working memory.

Space and time can each act as scaffolds for the individuation and selection of visual objects in working memory. Here we ask whether there is a trade-off between the use of space and time for visual working memory: whether observers will rely less on space, when memoranda can additionally be individuated through time. We tracked the use of space through directional biases in microsaccades after attention was directed to memory contents that had been encoded simultaneously or sequentially to the left and right of fixation. We found that spatial gaze biases were preserved when participants could (Experiment 1) and even when they had to (Experiment 2) additionally rely on time for object individuation. Thus, space remains a profound organizing medium for working memory even when other organizing sources are available and utilized, with no evidence for an obligatory trade-off between the use of space and time.

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.

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.

Functional but not obligatory link between microsaccades and neural modulation by covert spatial attention.

Covert spatial attention is associated with spatial modulation of neural activity as well as with directional biases in fixational eye movements known as microsaccades. We studied how these two 'fingerprints' of attention are interrelated in humans. We investigated spatial modulation of 8-12 Hz EEG alpha activity and microsaccades when attention is directed internally within the spatial layout of visual working memory. Consistent with a common origin, spatial modulations of alpha activity and microsaccades co-vary: alpha lateralisation is stronger in trials with microsaccades toward versus away from the memorised location of the to-be-attended item and occurs earlier in trials with earlier microsaccades toward this item. Critically, however, trials without attention-driven microsaccades nevertheless show clear spatial modulation of alpha activity - comparable to trials with attention-driven microsaccades. Thus, directional biases in microsaccades correlate with neural signatures of spatial attention, but they are not necessary for neural modulation by spatial attention to be manifest.

Transient beta activity and cortico-muscular connectivity during sustained motor behaviour.

Neural oscillations are thought to play a central role in orchestrating activity states between distant neural populations. For example, during isometric contraction, 13-30 Hz beta activity becomes phase coupled between the motor cortex and the contralateral muscle. This and related observations have led to the proposal that beta activity and connectivity sustain stable cognitive and motor states - or the 'status quo' - in the brain. Recently, however, beta activity at the single-trial level has been shown to be short-lived - though so far this has been reported for regional beta activity in tasks without sustained motor demands. Here, we measured magnetoencephalography (MEG) and electromyography (EMG) in 18 human participants performing a sustained isometric contraction (gripping) task. If cortico-muscular beta connectivity is directly responsible for sustaining a stable motor state, then beta activity within single trials should be (or become) sustained in this context. In contrast, we found that motor beta activity and connectivity with the downstream muscle were transient. Moreover, we found that sustained motor requirements did not prolong beta-event duration in comparison to rest. These findings suggest that neural synchronisation between the brain and the muscle involves short 'bursts' of frequency-specific connectivity, even when task demands - and motor behaviour - are sustained.

Consequences of predictable temporal structure in multi-task situations.

In everyday life, we often anticipate the timing of an upcoming task or event while actively engaging in another. Here, we investigated the effects of predictable temporal structure within such a multi-task scenario. In a visual working-memory task, we manipulated whether the onset of a working-memory probe could be predicted in time, while also embedding a simple intervening task within the delay period. We first show that working-memory performance benefitted from temporal expectations, even though an intervening task had to be completed in the interim. Moreover, temporal predictions regarding the upcoming working-memory probe additionally affected performance on the intervening task, resulting in faster responses when the memory probe was expected early, and slower responses when the memory probe was expected late, as compared to when it was temporally unpredictable. Because the intervening task always occurred at the same time during the memory delay, differences in performance on this intervening task result from a between-task consequence of temporal expectation. Thus, we show that within multi-task settings, knowing when working-memory contents will be required for an upcoming task not only facilitates performance of the associated working-memory task, but can also influence the performance of other, intervening tasks.

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.

Multiple spatial frames for immersive working memory.

As we move around, relevant information that disappears from sight can still be held in working memory to serve upcoming behaviour. How we maintain and select visual information as we move through the environment remains poorly understood because most laboratory tasks of working memory rely on removing visual material while participants remain still. We used virtual reality to study visual working memory following self-movement in immersive environments. Directional biases in gaze revealed the recruitment of more than one spatial frame for maintaining and selecting memoranda following self-movement. The findings bring the important realization that multiple spatial frames support working memory in natural behaviour. The results also illustrate how virtual reality can be a critical experimental tool to characterize this core memory system.