Internal attention modulates the functional state of novel stimulus-response associations in working memory.

Information in working memory (WM) is crucial for guiding behavior. However, not all WM representations are equally relevant simultaneously. Current theoretical frameworks propose a functional dissociation between 'latent' and 'active' states, in which relevant representations are prioritized into an optimal (active) state to face current demands, while relevant information that is not immediately needed is maintained in a dormant (latent) state. In this context, task demands can induce rapid and flexible prioritization of information from latent to active state. Critically, these functional states have been primarily studied using simple visual memories, with attention selecting and prioritizing relevant representations to serve as templates to guide subsequent behavior. It remains unclear whether more complex WM representations, such as novel stimulus-response associations, can also be prioritized into different functional states depending on their task relevance, and if so how these different formats relate to each other. In the present study, we investigated whether novel WM-guided actions can be brought into different functional states depending on current task demands. Our results reveal that planned actions can be flexibly prioritized when needed and show how their functional state modulates their influence on ongoing behavior. Moreover, they suggest the representations of novel actions of different functional states are maintained in WM via a non-orthogonal coding scheme, thus are prone to interference.

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.

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.

Considering Readout to Understand Working Memory.

While working memory (WM) allows us to store past information, its function is to guide future behavior. Given this role, the tight link between how WMs are maintained and how they are read out to be transformed into context-appropriate actions remains relatively unexplored. Beyond helping us understand memory-guided behavior, focusing on WM readout may also help us better understand the neural basis of memory maintenance.

Neural Reinstatement Tracks Spread of Attention between Object Features in Working Memory.

Attention can be allocated in working memory (WM) to select and privilege relevant content. It is unclear whether attention selects individual features or whole objects in WM. Here, we used behavioral measures, eye-tracking, and EEG to test the hypothesis that attention spreads between an object's features in WM. Twenty-six participants completed a WM task that asked them to recall the angle of one of two oriented, colored bars after a delay while EEG and eye-tracking data were collected. During the delay, an orthogonal "incidental task" cued the color of one item for a match/mismatch judgment. On congruent trials (50%), the cued item was probed for subsequent orientation recall; on incongruent trials (50%), the other memory item was probed. As predicted, selecting the color of an object in WM brought other features of the cued object into an attended state as revealed by EEG decoding, oscillatory α-power, gaze bias, and improved orientation recall performance. Together, the results show that attentional selection spreads between an object's features in WM, consistent with object-based attentional selection. Analyses of neural processing at recall revealed that the selected object was automatically compared with the probe, whether it was the target for recall or not. This provides a potential mechanism for the observed benefits of nonpredictive cueing in WM, where a selected item is prioritized for subsequent decision-making.

Integrating Reward Information for Prospective Behavior.

Value-based decision-making is often studied in a static context, where participants decide which option to select from those currently available. However, everyday life often involves an additional dimension: deciding when to select to maximize reward. Recent evidence suggests that agents track the latent reward of an option, updating changes in their latent reward estimate, to achieve appropriate selection timing (latent reward tracking). However, this strategy can be difficult to distinguish from one in which the optimal selection time is estimated in advance, allowing an agent to wait a predetermined amount of time before selecting, without needing to monitor an option's latent reward (distance-to-goal tracking). Here, we show that these strategies can in principle be dissociated. Human brain activity was recorded using electroencephalography (EEG), while female and male participants performed a novel decision task. Participants were shown an option and decided when to select it, as its latent reward changed from trial-to-trial. While the latent reward was uncued, it could be estimated using cued information about the option's starting value and value growth rate. We then used representational similarity analysis (RSA) to assess whether EEG signals more closely resembled latent reward tracking or distance-to-goal tracking. This approach successfully dissociated the strategies in this task. Starting value and growth rate were translated into a distance-to-goal signal, far in advance of selecting the option. Latent reward could not be independently decoded. These results demonstrate the feasibility of using high temporal resolution neural recordings to identify internally computed decision variables in the human brain.SIGNIFICANCE STATEMENT Reward-seeking behavior involves acting at the right time. However, the external world does not always tell us when an action is most rewarding, necessitating internal representations that guide action timing. Specifying this internal neural representation is challenging because it might stem from a variety of strategies, many of which make similar predictions about brain activity. This study used a novel approach to test whether alternative strategies could be dissociated in principle. Using representational similarity analysis (RSA), we were able to distinguish between candidate internal representations for selection timing. This shows how pattern analysis methods can be used to measure latent decision information in noninvasive neural data.

Gender bias in academia: A lifetime problem that needs solutions.

Despite increased awareness of the lack of gender equity in academia and a growing number of initiatives to address issues of diversity, change is slow, and inequalities remain. A major source of inequity is gender bias, which has a substantial negative impact on the careers, work-life balance, and mental health of underrepresented groups in science. Here, we argue that gender bias is not a single problem but manifests as a collection of distinct issues that impact researchers' lives. We disentangle these facets and propose concrete solutions that can be adopted by individuals, academic institutions, and society.

A Hierarchy of Functional States in Working Memory.

Extensive research has examined how information is maintained in working memory (WM), but it remains unknown how WM is used to guide behavior. We addressed this question by combining human electrophysiology (50 subjects, male and female) with pattern analyses, cognitive modeling, and a task requiring the prolonged maintenance of two WM items and priority shifts between them. This enabled us to discern neural states coding for memories that were selected to guide the next decision from states coding for concurrently held memories that were maintained for later use, and to examine how these states contribute to WM-based decisions. Selected memories were encoded in a functionally active state. This state was reflected in spontaneous brain activity during the delay period, closely tracked moment-to-moment fluctuations in the quality of evidence integration, and also predicted when memories would interfere with each other. In contrast, concurrently held memories were encoded in a functionally latent state. This state was reflected only in stimulus-evoked brain activity, tracked memory precision at longer timescales, but did not engage with ongoing decision dynamics. Intriguingly, the two functional states were highly flexible, as priority could be dynamically shifted back and forth between memories without degrading their precision. These results delineate a hierarchy of functional states, whereby latent memories supporting general maintenance are transformed into active decision circuits to guide flexible behavior.SIGNIFICANCE STATEMENT Working memory enables maintenance of information that is no longer available in the environment. Abundant neuroscientific work has examined where in the brain working memories are stored, but it remains unknown how they are represented and used to guide behavior. Our study shows that working memories are represented in qualitatively different formats, depending on behavioral priorities. Memories that are selected for guiding behavior are encoded in an active state that transforms sensory input into decision variables, whereas other concurrently held memories are encoded in a latent state that supports precise maintenance without affecting ongoing cognition. These results dissociate mechanisms supporting memory storage and usage, and open the door to reveal not only where memories are stored but also how.

Theoretical distinction between functional states in working memory and their corresponding neural states.

Working memory (WM) is important for guiding behaviour, but not always for the next possible action. Here we define a WM item that is currently relevant for guiding behaviour as the functionally "active" item; whereas items maintained in WM, but not immediately relevant to behaviour, are defined as functionally "latent". Traditional neurophysiological theories of WM proposed that content is maintained via persistent neural activity (e.g., stable attractors); however, more recent theories have highlighted the potential role for "activity-silent" mechanisms (e.g., short-term synaptic plasticity). Given these somewhat parallel dichotomies, functionally active and latent cognitive states of WM have been associated with storage based on persistent-activity and activity-silent neural mechanisms, respectively. However, in this article we caution against a one-to-one correspondence between functional and activity states. We argue that the principal theoretical requirement for active and latent WM is that the corresponding neural states play qualitatively different functional roles. We consider a number of candidate solutions, and conclude that the neurophysiological mechanisms for functionally active and latent WM items are theoretically independent of the distinction between persistent activity-based and activity-silent forms of WM storage.

Rhythmic Temporal Expectation Boosts Neural Activity by Increasing Neural Gain.

Temporal orienting improves sensory processing, akin to other top-down biases. However, it is unknown whether these improvements reflect increased neural gain to any stimuli presented at expected time points, or specific tuning to task-relevant stimulus aspects. Furthermore, while other top-down biases are selective, the extent of trade-offs across time is less well characterized. Here, we tested whether gain and/or tuning of auditory frequency processing in humans is modulated by rhythmic temporal expectations, and whether these modulations are specific to time points relevant for task performance. Healthy participants (N = 23) of either sex performed an auditory discrimination task while their brain activity was measured using magnetoencephalography/electroencephalography (M/EEG). Acoustic stimulation consisted of sequences of brief distractors interspersed with targets, presented in a rhythmic or jittered way. Target rhythmicity not only improved behavioral discrimination accuracy and M/EEG-based decoding of targets, but also of irrelevant distractors preceding these targets. To explain this finding in terms of increased sensitivity and/or sharpened tuning to auditory frequency, we estimated tuning curves based on M/EEG decoding results, with separate parameters describing gain and sharpness. The effect of rhythmic expectation on distractor decoding was linked to gain increase only, suggesting increased neural sensitivity to any stimuli presented at relevant time points.SIGNIFICANCE STATEMENT Being able to predict when an event may happen can improve perception and action related to this event, likely due to the alignment of neural activity to the temporal structure of stimulus streams. However, it is unclear whether rhythmic increases in neural sensitivity are specific to task-relevant targets, and whether they competitively impair stimulus processing at unexpected time points. By combining magnetoencephalography and encephalographic recordings, neural decoding of auditory stimulus features, and modeling, we found that rhythmic expectation improved neural decoding of both relevant targets and irrelevant distractors presented and expected time points, but did not competitively impair stimulus processing at unexpected time points. Using a quantitative model, these results were linked to nonspecific neural gain increases due to rhythmic expectation.

Reward Boosts Neural Coding of Task Rules to Optimize Cognitive Flexibility.

Cognitive flexibility is critical for intelligent behavior. However, its execution is effortful and often suboptimal. Recent work indicates that flexible behavior can be improved by the prospect of reward, which suggests that rewards optimize flexible control processes. Here we investigated how different reward prospects influence neural encoding of task rule information to optimize cognitive flexibility. We applied representational similarity analysis to human electroencephalograms, recorded while female and male participants performed a rule-guided decision-making task. During the task, the prospect of reward varied from trial to trial. Participants made faster, more accurate judgements on high-reward trials. Critically, high reward boosted neural coding of the active task rule, and the extent of this increase was associated with improvements in task performance. Additionally, the effect of high reward on task rule coding was most pronounced on switch trials, where rules were updated relative to the previous trial. These results suggest that reward prospect can promote cognitive performance by strengthening neural coding of task rule information, helping to improve cognitive flexibility during complex behavior.SIGNIFICANCE STATEMENT The importance of motivation is evident in the ubiquity with which reward prospect guides adaptive behavior and the striking number of neurological conditions associated with motivational impairments. In this study, we investigated how dynamic changes in motivation, as manipulated through reward, shape neural coding for task rules during a flexible decision-making task. The results of this work suggest that motivation to obtain reward modulates the encoding of task rules needed for flexible behavior. The extent to which reward increased task rule coding also tracked improvements in behavioral performance under high-reward conditions. These findings help to inform how motivation shapes neural processing in the healthy human brain.

Neural markers of category-based selective working memory in aging.

Working memory (WM) is essential for normal cognitive function, but shows marked decline in aging. The importance of selective attention in guiding WM performance is increasingly recognized. Studies so far are inconclusive about the ability to use selective attention during WM in aging. To investigate the neural mechanisms supporting selective attention in WM in aging, we tested a large group of older adults using functional magnetic resonance imaging whilst they performed a category-based (faces/houses) selective-WM task. Older adults were able to use attention to encode targets and suppress distractors to reach high levels of task performance. A subsequent, surprise recognition-memory task showed strong consequences of selective attention. Attended items in the relevant category were recognized significantly better than items in the ignored category. Neural measures also showed reliable markers of selective attention during WM. Purported control regions including the dorsolateral and inferior prefrontal and anterior cingulate cortex were reliably recruited for attention to both categories. Activation levels in category-sensitive visual cortex showed reliable modulation according to attentional demands, and positively correlated with subsequent memory measures of attention and WM span. Psychophysiological interaction analyses showed that activity in category-sensitive areas were coupled with non-sensory cortex known to be involved in cognitive control and memory processing, including regions in the prefrontal cortex and hippocampus. In summary, we found that older adults were able to recruit a network of brain regions involved in top-down attention during selective WM, and individual differences in attentional control corresponded to the degree of attention-related modulation in the brain.

Temporally Unconstrained Decoding Reveals Consistent but Time-Varying Stages of Stimulus Processing.

In this article, we propose a method to track trial-specific neural dynamics of stimulus processing and decision making with high temporal precision. By applying this novel method to a perceptual template-matching task, we tracked representational brain states associated with the cascade of neural processing, from early sensory areas to higher order areas that are involved in integration and decision making. We address a major limitation of the traditional decoding approach: that it relies on consistent timing of these processes over trials. Using a TUDA approach, we found that the timing of the cognitive processes involved in perceptual judgments can vary considerably over trials. This revealed that the sequence of processing states was consistent for all subjects and trials, even when the timing of these states varied. Furthermore, we found that the specific timing of states on each trial was related to the quality of performance over trials. Altogether, this work not only highlights the serious pitfalls and misleading interpretations that result from assuming stimulus processing to be synchronous across trials but can also open important avenues to investigate learning and quantify plasticity.

Benefits of flexible prioritization in working memory can arise without costs.

Most recent models conceptualize working memory (WM) as a continuous resource, divided up according to task demands. When an increasing number of items need to be remembered, each item receives a smaller chunk of the memory resource. These models predict that the allocation of attention to high-priority WM items during the retention interval should be a zero-sum game: improvements in remembering cued items come at the expense of uncued items because resources are dynamically transferred from uncued to cued representations. The current study provides empirical data challenging this model. Four precision retrocueing WM experiments assessed cued and uncued items on every trial. This permitted a test for trade-off of the memory resource. We found no evidence for trade-offs in memory across trials. Moreover, robust improvements in WM performance for cued items came at little or no cost to uncued items that were probed afterward, thereby increasing the net capacity of WM relative to neutral cueing conditions. An alternative mechanism of prioritization proposes that cued items are transferred into a privileged state within a response-gating bottleneck, in which an item uniquely controls upcoming behavior. We found evidence consistent with this alternative. When an uncued item was probed first, report of its orientation was biased away from the cued orientation to be subsequently reported. We interpret this bias as competition for behavioral control in the output-driving bottleneck. Other items in WM did not bias each other, making this result difficult to explain with a shared resource model. (PsycINFO Database Record

Individual Correspondence of Amyloid-ß and Intrinsic Connectivity in the Posterior Default Mode Network Across Stages of Alzheimer's Disease.

In Alzheimer's disease (AD), amyloid-ß (Aß) pathology and intrinsic functional connectivity (iFC) interact. Across stages of AD, we expected individual spatial correspondence of Aß and iFC to reveal both Aß accumulation and its detrimental effects on iFC. We used resting-state functional magnetic imaging and Aß imaging in a cross-sectional sample of 90 subjects across stages of AD and healthy older adults. Global and local correspondence of Aß and iFC were assessed within the posterior default mode network (pDMN) by within-subject voxel-wise correlations. Beginning at preclinical stages, global Aß-iFC correspondence was positive for the whole pDMN, showing that Aß accumulates in areas of high connectivity, and reached a plateau at prodromal stages. Starting at preclinical stages, local correspondence was negative in network centers, indicating that Aß reduces connectivity of the pDMN as a function of local plaque concentration, and peaked at prodromal stages. Positive global correspondence suggests that Aß accumulation progresses along iFC, with this effect starting in preclinical stages, and being constant along clinical periods. Negative local correspondence suggests detrimental effects of Aß on iFC in network centers, starting at preclinical stages, and peaking when first symptoms appear. Data reveal a complex trajectory of Aß and iFC correspondence, affecting both Aß accumulation and iFC impairments.

Prioritizing Information during Working Memory: Beyond Sustained Internal Attention.

Working memory (WM) has limited capacity. This leaves attention with the important role of allowing into storage only the most relevant information. It is increasingly evident that attention is equally crucial for prioritizing representations within WM as the importance of individual items changes. Retrospective prioritization has been proposed to result from a focus of internal attention highlighting one of several representations. Here, we suggest an updated model, in which prioritization acts in multiple steps: first orienting towards and selecting a memory, and then reconfiguring its representational state in the service of upcoming task demands. Reconfiguration sets up an optimized perception-action mapping, obviating the need for sustained attention. This view is consistent with recent literature, makes testable predictions, and links WM with task switching and action preparation.

Increased Intrinsic Activity of Medial-Temporal Lobe Subregions is Associated with Decreased Cortical Thickness of Medial-Parietal Areas in Patients with Alzheimer's Disease Dementia.

In Alzheimer's disease (AD), disrupted connectivity between medial-parietal cortices and medial-temporal lobes (MTL) is linked with increased MTL local functional connectivity, and parietal atrophy is associated with increased MTL memory activation. We hypothesized that intrinsic activity in MTL subregions is increased and associated with medial-parietal degeneration and impaired memory in AD. To test this hypothesis, resting-state-functional and structural-MRI was assessed in 22 healthy controls, 22 mild cognitive impairment patients, and 21 AD-dementia patients. Intrinsic activity was measured by power-spectrum density of blood-oxygenation-level-dependent signal, medial-parietal degeneration by cortical thinning. In AD-dementia patients, intrinsic activity was increased for several right MTL subregions. Raised intrinsic activity in dentate gyrus and cornu ammonis 1 was associated with cortical thinning in posterior cingulate cortices, and at-trend with impaired delayed recall. Critically, increased intrinsic activity in the right entorhinal cortex was associated with ipsilateral posterior cingulate degeneration. Our results provide evidence that in AD, intrinsic activity in MTL subregions is increased and associated with medial-parietal atrophy. Results fit a model in which medial-parietal degeneration contributes to MTL dysconnectivity from medial-parietal cortices, potentially underpinning disinhibition-like changes in MTL activity.

Behavioral and Neural Markers of Flexible Attention over Working Memory in Aging.

Working memory (WM) declines as we age and, because of its fundamental role in higher order cognition, this can have highly deleterious effects in daily life. We investigated whether older individuals benefit from flexible orienting of attention within WM to mitigate cognitive decline. We measured magnetoencephalography (MEG) in older adults performing a WM precision task with cues during the maintenance period that retroactively predicted the location of the relevant items for performance (retro-cues). WM performance of older adults significantly benefitted from retro-cues. Whereas WM maintenance declined with age, retro-cues conferred strong attentional benefits. A model-based analysis revealed an increase in the probability of recalling the target, a lowered probability of retrieving incorrect items or guessing, and an improvement in memory precision. MEG recordings showed that retro-cues induced a transient lateralization of alpha (8-14 Hz) and beta (15-30 Hz) oscillatory power. Interestingly, shorter durations of alpha/beta lateralization following retro-cues predicted larger cueing benefits, reinforcing recent ideas about the dynamic nature of access to WM representations. Our results suggest that older adults retain flexible control over WM, but individual differences in control correspond to differences in neural dynamics, possibly reflecting the degree of preservation of control in healthy aging.

Tracking the changing feature of a moving object.

The mind can track not only the changing locations of moving objects, but also their changing features, which are often meaningful for guiding action. How does the mind track such features? Using a task in which observers tracked the changing orientation of a rolling wheel's spoke, we found that this ability is enabled by a highly feature-specific process which continuously tracks the orientation feature itself--even during occlusion, when the feature is completely invisible. This suggests that the mental representation of a changing orientation feature and its moving object are continuously transformed and updated, akin to studies showing continuous tracking of an object's boundaries alone. We also found a systematic error in performance, whereby the orientation was reliably perceived to be further ahead than it truly was. This effect appears to occur because during occlusion the mental representation of the feature is transformed beyond the veridical position, perhaps in order to conservatively anticipate future feature states.

Testing sensory evidence against mnemonic templates.

Most perceptual decisions require comparisons between current input and an internal template. Classic studies propose that templates are encoded in sustained activity of sensory neurons. However, stimulus encoding is itself dynamic, tracing a complex trajectory through activity space. Which part of this trajectory is pre-activated to reflect the template? Here we recorded magneto- and electroencephalography during a visual target-detection task, and used pattern analyses to decode template, stimulus, and decision-variable representation. Our findings ran counter to the dominant model of sustained pre-activation. Instead, template information emerged transiently around stimulus onset and quickly subsided. Cross-generalization between stimulus and template coding, indicating a shared neural representation, occurred only briefly. Our results are compatible with the proposal that template representation relies on a matched filter, transforming input into task-appropriate output. This proposal was consistent with a signed difference response at the perceptual decision stage, which can be explained by a simple neural model.