Bend but don't break: Prioritization protects working memory from displacement but leaves it vulnerable to distortion from distraction.

Perceptual distraction distorts visual working memory representations. Previous research has shown that memory responses are systematically biased towards passively viewed visual distractors that are similar to the memoranda. However, it remains unclear whether the prioritization of one working memory representation over another reduces the impact of perceptual distractors. We designed a study with five different types of visual distraction that varied in engagement and found evidence for both subtle distortions and catastrophic failures of memory. Importantly, prioritization protected working memories from catastrophic loss (fewer "swap errors") but rendered them more vulnerable to distortion (greater attractive "biases" towards the distractor). Our findings demonstrate that prioritization does not simply protect working memory from any and all interference, but rather it reduces the likelihood of catastrophic disruption from perceptual distraction at the cost of an increased likelihood of distortion.

Rumination burdens the updating of working memory.

Working memory is a vital, but capacity-limited, cognitive instrument that requires frequent updating as our goals and environment change. Individuals diagnosed with depression have a reduced capacity compared with the general population, as they have a propensity to fixate on negative information, even when it is not relevant for the task at hand. Here we investigated how characteristics of psychiatric illnesses, such as rumination, affect a person's ability to efficiently update emotional information in mind. We used both neutral and negative pictures of scenes in a working memory updating task that required participants to occasionally replace items held in mind during a brief delay period. Participants were presented with a probe item at the end of each trial and asked to report whether that item was in their current memory set. Responses were slowest and least accurate for images that had been replaced (i.e., "lures"), indicating there was some difficulty in successfully updating working memory in this paradigm. Participants who have both a high propensity to ruminate and a low working memory capacity were significantly more likely to false alarm to these lures. While emotional valence did not impact accuracy for these participants, their false alarms were faster for negative stimuli compared with neutral stimuli, indicating that task-irrelevant emotional information was more difficult to remove from working memory. These results demonstrate how rumination impairs goal-directed behavior by obscuring the boundary between relevant and irrelevant information in working memory.

Prioritization sharpens working memories but does not protect them from distraction.

Perceptual distraction distorts visual working memory representations. Previous research has shown that memory responses are systematically biased toward visual distractors that are similar to the memoranda. However, it remains unclear whether the prioritization of one working memory representation over another reduces the impact of perceptual distractors. In five behavioral experiments, we used different forms of retrospective cues (indicating the likelihood of testing each item and/or the reward for responding correctly to each item) to manipulate the prioritization of items in working memory before visual distraction. We examined the effects of distraction with nonparametric analyses and a novel distractor intrusion model. We found that memory responses were more precise (lower absolute response errors and stronger memory signals) for items that were prioritized. However, these prioritized items were not immune to distraction, and their memory responses were biased toward the visual distractors to the same degree as were unprioritized items. Our findings demonstrate that the benefits associated with prioritization in working memory do not include protection from distraction biases. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Pattern analysis of neuroimaging data reveals novel insights on threat learning and extinction in humans.

Several decades of rodent neurobiology research have identified a network of brain regions that support Pavlovian threat conditioning and extinction, focused predominately on the amygdala, hippocampus, and medial prefrontal cortex (mPFC). Surprisingly, functional magnetic resonance imaging (fMRI) studies have shown inconsistent evidence for these regions while humans undergo threat conditioning and extinction. In this review, we suggest that translational neuroimaging efforts have been hindered by reliance on traditional univariate analysis of fMRI. Whereas univariate analyses average activity across voxels in a given region, multivariate pattern analyses (MVPA) leverage the information present in spatial patterns of activity. MVPA therefore provides a more sensitive analysis tool to translate rodent neurobiology to human neuroimaging. We review human fMRI studies using MVPA that successfully bridge rodent models of amygdala, hippocampus, and mPFC function during Pavlovian learning. We also highlight clinical applications of these information-sensitive multivariate analyses. In sum, we advocate that the field should consider adopting a variety of multivariate approaches to help bridge cutting-edge research on the neuroscience of threat and anxiety.

Rewarded Extinction Increases Amygdalar Connectivity and Stabilizes Long-Term Memory Traces in the vmPFC.

Neurobiological evidence in rodents indicates that threat extinction incorporates reward neurocircuitry. Consequently, incorporating reward associations with an extinction memory may be an effective strategy to persistently attenuate threat responses. Moreover, while there is considerable research on the short-term effects of extinction strategies in humans, the long-term effects of extinction are rarely considered. In a within-subjects fMRI study with both female and male participants, we compared counterconditioning (CC; a form of rewarded-extinction) to standard extinction at recent (24 h) and remote (approximately one month) retrieval tests. Relative to standard extinction, rewarded extinction diminished 24-h relapse of arousal and threat expectancy, and reduced activity in brain regions associated with the appraisal and expression of threat (e.g., thalamus, insula, periaqueductal gray). The retrieval of reward-associated extinction memory was accompanied by functional connectivity between the amygdala and the ventral striatum, whereas the retrieval of standard-extinction memories was associated with connectivity between the amygdala and ventromedial prefrontal cortex (vmPFC). One month later, the retrieval of both standard-extinction and rewarded-extinction was associated with amygdala-vmPFC connectivity. However, only rewarded extinction created a stable memory trace in the vmPFC, identified through overlapping multivariate patterns of fMRI activity from extinction to 24-h and one-month retrieval. These findings provide new evidence that reward may generate a more stable and enduring memory trace of attenuated threat in humans.SIGNIFICANCE STATEMENT Prevalent treatments for pathologic fear and anxiety are based on the principles of Pavlovian extinction. Unfortunately, extinction forms weak memories that only temporarily inhibit the retrieval of threat associations. Thus, to increase the translational relevance of extinction research, it is critical to investigate whether extinction can be augmented to form a more enduring memory, especially after long intervals. Here, we used a multiday fMRI paradigm in humans to compare the short-term and long-term neurobehavioral effects of aversive-to-appetitive counterconditioning (CC), a form of augmented extinction. Our results provide novel evidence that including an appetitive stimulus during extinction can reduce short-term threat relapse and stabilize the memory trace of extinction in the ventromedial prefrontal cortex (vmPFC), for at least one month after learning.

Distinct monitoring strategies underlie costs and performance in prospective memory.

Prospective memory (PM) describes the ability to remember to perform goal-relevant actions at an appropriate time in the future amid concurrent demands. A key contributor to PM performance is thought to be the effortful monitoring of the environment for PM-related cues, a process whose existence is typically inferred from a behavioral interference measure of reaction times. This measure, referred to as "PM costs," is an informative but indirect proxy for monitoring, and it may not be sufficient to understand PM behaviors in all situations. In this study, we asked participants to perform a visual search task with arrows that varied in difficulty while concurrently performing a delayed-recognition PM task with pictures of faces and scenes. To gain a precise measurement of monitoring behavior, we used eye-tracking to record fixations to all task-relevant stimuli and related these fixation measures to both PM costs and PM accuracy. We found that PM costs reflected dissociable monitoring strategies: higher costs were associated with early and frequent monitoring while lower costs were associated with delayed and infrequent monitoring. Moreover, the link between fixations and PM costs varied with cognitive load, and the inclusion of fixation data yielded better predictions of PM accuracy than using PM costs alone. This study demonstrates the benefit of eye-tracking to disentangle the nature of PM costs and more precisely describe strategies involved in prospective remembering.

Working Memory Swap Errors Have Identifiable Neural Representations.

Working memory is an essential component of cognition that facilitates goal-directed behavior. Famously, it is severely limited and performance suffers when memory load exceeds an individual's capacity. Modeling of visual working memory responses has identified two likely types of errors: guesses and swaps. Swap errors may arise from a misbinding between the features of different items. Alternatively, these errors could arise from memory noise in the feature dimension used for cueing a to-be-tested memory item, resulting in the wrong item being selected. Finally, it is possible that so-called swap errors actually reflect informed guessing, which could occur at the time of a cue, or alternatively, at the time of the response. Here, we combined behavioral response modeling and fMRI pattern analysis to test the hypothesis that swap errors involve the active maintenance of an incorrect memory item. After the encoding of six spatial locations, a retro-cue indicated which location would be tested after memory retention. On accurate trials, we could reconstruct a memory representation of the cued location in both early visual cortex and intraparietal sulcus. On swap error trials identified with mixture modeling, we were able to reconstruct a representation of the swapped location, but not of the cued location, suggesting the maintenance of the incorrect memory item before response. Moreover, participants subjectively responded with some level of confidence, rather than complete guessing, on a majority of swap error trials. Together, these results suggest that swap errors are not mere response-phase guesses, but instead result from failures of selection in working memory, contextual binding errors, or informed guesses, which produce active maintenance of incorrect memory representations.

Neural reinstatement reveals divided organization of fear and extinction memories in the human brain.

Neurobiological research in rodents has revealed that competing experiences of fear and extinction are stored as distinct memory traces in the brain. This divided organization is adaptive for mitigating overgeneralization of fear to related stimuli that are learned to be safe while also maintaining threat associations for unsafe stimuli. The mechanisms involved in organizing these competing memories in the human brain remain unclear. Here, we used a hybrid form of Pavlovian conditioning with an episodic memory component to identify overlapping multivariate patterns of fMRI activity associated with the formation and retrieval of fear versus extinction. In healthy adults, distinct regions of the medial prefrontal cortex (PFC) and hippocampus showed selective reactivation of fear versus extinction memories based on the temporal context in which these memories were encoded. This dissociation was absent in participants with posttraumatic stress disorder (PTSD) symptoms. The divided neural organization of fear and extinction may support flexible retrieval of context-appropriate emotional memories, while their disorganization may promote overgeneralization and increased fear relapse in affective disorders.

Estimating Intrinsic Manifold Dimensionality to Classify Task-Related Information in Human and Non-Human Primate Data.

Feature selection, or dimensionality reduction, has become a standard step in reducing large-scale neural datasets into usable signals for brain-machine interface and neurofeedback decoders. Current techniques in fMRI data reduce the number of voxels (features) by performing statistics on individual voxels or using traditional techniques that utilize linear combinations of features (e.g., principal component analysis (PCA)). However, these methods often do not account for the cross-correlations found across voxels and do not sufficiently reduce the feature space to support efficient real-time feedback. To overcome these limitations, we propose using factor analysis on fMRI data. This technique has become increasingly popular for extracting a minimal number of latent features to explain high-dimensional data in non-human primates (NHPs). Here, we demonstrate these methods in both NHP and human data. In NHP subjects (n=2), we reduced the number of features to an average of 26.86% and 14.86% of the total feature space to build our multinomial classifier. In one NHP subject, the average accuracy of classifying eight target locations over 64 sessions was 62.43% (+/-6.19%) compared to a PCA-based classifier with 60.26% (+/-6.02%). In healthy fMRI subjects, we reduced the feature space to an average of 0.33% of the initial space. Group average (n=5) accuracy of FA-based category classification was 74.33% (+/- 4.91%) compared to a PCA-based classifier with 68.42% (+/-4.79%). FA-based classifiers can maintain the performance fidelity observed with PCA-based decoders. Importantly, FA-based methods allow researchers to address specific hypotheses about how underlying neural activity relates to behavior.

Emotional learning retroactively enhances item memory but distorts source attribution.

An adaptive memory system should prioritize information surrounding a powerful learning event that may prove useful for predicting future meaningful events. The behavioral tagging hypothesis provides a mechanistic framework to interpret how weak experiences persist as durable memories through temporal association with a strong experience. Memories are composed of multiple elements, and different mnemonic aspects of the same experience may be uniquely affected by mechanisms that retroactively modulate a weakly encoded memory. Here, we investigated how emotional learning affects item and source memory for related events encoded close in time. Participants encoded trial-unique category exemplars before, during, and after Pavlovian fear conditioning. Selective retroactive enhancements in 24-h item memory were accompanied by a bias to misattribute items to the temporal context of fear conditioning. The strength of this source memory bias correlated with participants' retroactive item memory enhancement, and source misattribution to the emotional context predicted whether items were remembered overall. In the framework of behavioral tagging: Memory attribution was biased to the temporal context of the stronger event that provided the putative source of memory stabilization for the weaker event. We additionally found that fear conditioning selectively and retroactively enhanced stimulus typicality ratings for related items, and that stimulus typicality also predicted overall item memory. Collectively, these results provide new evidence that items related to emotional learning are misattributed to the temporal context of the emotional event and judged to be more representative of their semantic category. Both processes may facilitate memory retrieval for related events encoded close in time.

Separation of item and context in item-method directed forgetting.

Contextual information plays a critical role in directed forgetting (DF) of lists of items, whereas DF of individual items has been primarily associated with item-level processing. This study was designed to investigate whether context processing also contributes to the forgetting of individual items. Participants first viewed a series of words, with task-irrelevant scene images (used as "context tags") interspersed between them. Later, these words reappeared without the scenes and were followed by an instruction to remember or forget that word. Multivariate pattern analyses of fMRI data revealed that the reactivation of context information associated with the studied words (i.e., scene-related activity) was greater whereas the item-related information diminished after a forget instruction compared to a remember instruction. Critically, we found the magnitude of the separation between item information and context information predicted successful forgetting. These results suggest that the unbinding of an item from its context may support the intention to forget, and more generally they establish that contextual processing indeed contributes to item-method DF.

Distraction in Visual Working Memory: Resistance is Not Futile.

Over half a century of research focused on understanding how working memory is capacity constrained has overshadowed the fact that it is also remarkably resistant to interference. Protecting goal-relevant information from distraction is a cornerstone of cognitive function that involves a multifaceted collection of control processes and storage mechanisms. Here, we discuss recent advances in cognitive psychology and neuroscience that have produced new insights into the nature of visual working memory and its ability to resist distraction. We propose that distraction resistance should be an explicit component in any model of working memory and that understanding its behavioral and neural correlates is essential for building a comprehensive understanding of real-world memory function.

Thought suppression inhibits the generalization of fear extinction.

A challenge for translating fear extinction research into clinical treatments for stress and anxiety disorders is that extinction learning tends not to generalize beyond the treatment context. This may be because the hippocampus limits the expression of extinction memories. Consequently, downregulating the hippocampus may help to promote the generalization of extinction learning. One nonpharmacological strategy to downregulate hippocampal activity in humans is motivated forgetting, in which a participant deliberately attempts to suppress the encoding and/or retrieval of episodic memories. Here, we evaluated whether this strategy could facilitate extinction generalization by augmenting extinction training with thought suppression. Participants were threat conditioned using two conditioned stimulus (CS) categories paired with an electrical shock. Subsequently, during extinction training, one CS category was accompanied by thought suppression. Participants were tested for extinction generalization 24h later with conceptual variations of the extinguished stimuli. Contrary to our prediction, we found that extinction training paired with thought suppression resulted in enhanced shock expectancy (i.e., worse generalization) relative to standard extinction. We conclude that thought suppression during memory encoding likely acts as an inhibitory cue that blocks the acquisition of extinction memories, and therefore may not be a viable tactic to promote extinction generalization in the treatment of anxiety disorders.

Toward a Compassionate Intersectional Neuroscience: Increasing Diversity and Equity in Contemplative Neuroscience.

Mindfulness and compassion meditation are thought to cultivate prosocial behavior. However, the lack of diverse representation within both scientific and participant populations in contemplative neuroscience may limit generalizability and translation of prior findings. To address these issues, we propose a research framework called Intersectional Neuroscience which adapts research procedures to be more inclusive of under-represented groups. Intersectional Neuroscience builds inclusive processes into research design using two main approaches: 1) community engagement with diverse participants, and 2) individualized multivariate neuroscience methods to accommodate neural diversity. We tested the feasibility of this framework in partnership with a diverse U.S. meditation center (East Bay Meditation Center, Oakland, CA). Using focus group and community feedback, we adapted functional magnetic resonance imaging (fMRI) screening and recruitment procedures to be inclusive of participants from various under-represented groups, including racial and ethnic minorities, gender and sexual minorities, people with disabilities, neuropsychiatric disorders, and/or lower income. Using person-centered screening and study materials, we recruited and scanned 15 diverse meditators (80% racial/ethnic minorities, 53% gender and sexual minorities). The participants completed the EMBODY task - which applies individualized machine learning algorithms to fMRI data - to identify mental states during breath-focused meditation, a basic skill that stabilizes attention to support interoception and compassion. All 15 meditators' unique brain patterns were recognized by machine learning algorithms significantly above chance levels. These individualized brain patterns were used to decode the internal focus of attention throughout a 10-min breath-focused meditation period, specific to each meditator. These data were used to compile individual-level attention profiles during meditation, such as the percentage time attending to the breath, mind wandering, or engaging in self-referential processing. This study provides feasibility of employing an intersectional neuroscience approach to include diverse participants and develop individualized neural metrics of meditation practice. Through inclusion of more under-represented groups while developing reciprocal partnerships, intersectional neuroscience turns the research process into an embodied form of social action.

Long-term memory guides resource allocation in working memory.

Working memory capacity is incredibly limited and thus it is important to use this resource wisely. Prior knowledge in long-term memory can aid in efficient encoding of information by allowing for the prioritization of novel stimuli over familiar ones. Here we used a full-report procedure in a visual working memory paradigm, where participants reported the location of six colored circles in any order, to examine the influence of prior information on resource allocation in working memory. Participants learned that one of the items appeared in a restricted range of locations, whereas the remaining items could appear in any location. We found that participants' memory performance benefited from learning this prior information. Specifically, response precision increased for all items when prior information was available for one of the items. Responses for both familiar and novel items were systematically ordered from highest to lowest precision. Participants tended to report the familiar item in the second half of the six responses and did so with greater precision than for novel items. Moreover, novel items that appeared near the center of the prior location were reported with worse precision than novel items that appeared elsewhere. This shows that people strategically allocated working memory resources by ignoring information that appeared in predictable locations and prioritizing the encoding of information that appeared in unpredictable locations. Together these findings demonstrate that people rely on long-term memory not only for remembering familiar items, but also for the strategic allocation of their limited capacity working memory resources.

Changes to information in working memory depend on distinct removal operations.

Holding information in working memory is essential for cognition, but removing unwanted thoughts is equally important. Here we use multivariate pattern analyses of brain activity to demonstrate the successful manipulation and removal of information from working memory using different strategies including suppressing a specific thought, replacing a thought with a different one, and clearing the mind of all thought. These strategies are supported by distinct brain regions and have differential consequences for allowing new information to be encoded.

Focus on the Breath: Brain Decoding Reveals Internal States of Attention During Meditation.

Meditation practices are often used to cultivate interoception or internally-oriented attention to bodily sensations, which may improve health via cognitive and emotional regulation of bodily signals. However, it remains unclear how meditation impacts internal attention (IA) states due to lack of measurement tools that can objectively assess mental states during meditation practice itself, and produce time estimates of internal focus at individual or group levels. To address these measurement gaps, we tested the feasibility of applying multi-voxel pattern analysis (MVPA) to single-subject fMRI data to: (1) learn and recognize internal attentional states relevant for meditation during a directed IA task; and (2) decode or estimate the presence of those IA states during an independent meditation session. Within a mixed sample of experienced meditators and novice controls (N = 16), we first used MVPA to develop single-subject brain classifiers for five modes of attention during an IA task in which subjects were specifically instructed to engage in one of five states [i.e., meditation-related states: breath attention, mind wandering (MW), and self-referential processing, and control states: attention to feet and sounds]. Using standard cross-validation procedures, MVPA classifiers were trained in five of six IA blocks for each subject, and predictive accuracy was tested on the independent sixth block (iterated until all volumes were tested, N = 2,160). Across participants, all five IA states were significantly recognized well above chance (>41% vs. 20% chance). At the individual level, IA states were recognized in most participants (87.5%), suggesting that recognition of IA neural patterns may be generalizable for most participants, particularly experienced meditators. Next, for those who showed accurate IA neural patterns, the originally trained classifiers were applied to a separate meditation run (10-min) to make an inference about the percentage time engaged in each IA state (breath attention, MW, or self-referential processing). Preliminary group-level analyses demonstrated that during meditation practice, participants spent more time attending to breath compared to MW or self-referential processing. This paradigm established the feasibility of using MVPA classifiers to objectively assess mental states during meditation at the participant level, which holds promise for improved measurement of internal attention states cultivated by meditation.

Contextual reinstatement promotes extinction generalization in healthy adults but not PTSD.

For episodic memories, reinstating the mental context of a past experience improves retrieval of memories formed during that experience. Does context reinstatement serve a similar role for implicit, associative memories such as fear and extinction? Here, we used a fear extinction paradigm to investigate whether the retrieval of extinction (safety) memories is associated with reactivation of the mental context from extinction memory formation. In a two-day Pavlovian conditioning, extinction, and renewal protocol, we collected functional MRI data while healthy adults and adults with PTSD symptoms learned that conditioned stimuli (CSs) signaled threat through association with an electrical shock. Following acquisition, conceptually related exemplars from the CS category no longer signaled threat (i.e., extinction). Critically, during extinction only, task-irrelevant stimuli were presented between each CS trial to serve as "context tags" for subsequent identification of the possible reinstatement of this extinction context during a test of fear renewal the next day. We found that healthy adults exhibited extinction context reinstatement, as measured via multivariate pattern analysis of fMRI data, in the medial temporal lobe that related to behavioral performance, such that greater reinstatement predicted CSs being rated as safe instead of threatening. Moreover, context reinstatement positively correlated with univariate activity in the ventromedial prefrontal cortex and hippocampus, regions which are thought to be important for extinction learning. These relationships were not observed in the PTSD symptom group. These findings provide new evidence of a contextual reinstatement mechanism that helps resolve competition between the retrieval of opposing associative memories of threat and safety in the healthy adult brain that is dysregulated in PTSD.

Consensus on the reporting and experimental design of clinical and cognitive-behavioural neurofeedback studies (CRED-nf checklist).

Neurofeedback has begun to attract the attention and scrutiny of the scientific and medical mainstream. Here, neurofeedback researchers present a consensus-derived checklist that aims to improve the reporting and experimental design standards in the field.

Distraction biases working memory for faces.

Working memory persists in the face of distraction, yet not without consequence. Previous research has shown that memory for low-level visual features is systematically influenced by the maintenance or presentation of a similar distractor stimulus. Responses are frequently biased in stimulus space towards a perceptual distractor, though this has yet to be determined for high-level stimuli. We investigated whether these influences are shared for complex visual stimuli such as faces. To quantify response accuracies for these stimuli, we used a delayed-estimation task with a computer-generated "face space" consisting of 80 faces that varied continuously as a function of age and sex. In a set of three experiments, we found that responses for a target face held in working memory were biased towards a distractor face presented during the maintenance period. The amount of response bias did not vary as a function of distance between target and distractor. Our data suggest that, similar to low-level visual features, high-level face representations in working memory are biased by the processing of related but task-irrelevant information.