Structured memory representations develop at multiple time scales in hippocampal-cortical networks.

Influential views of systems memory consolidation posit that the hippocampus rapidly forms representations of specific events, while neocortical networks extract regularities across events, forming the basis of schemas and semantic knowledge. Neocortical extraction of schematic memory representations is thought to occur on a protracted timescale of months, especially for information that is unrelated to prior knowledge. However, this theorized evolution of memory representations across extended timescales, and differences in the temporal dynamics of consolidation across brain regions, lack reliable empirical support. To examine the temporal dynamics of memory representations, we repeatedly exposed human participants to structured information via sequences of fractals, while undergoing longitudinal fMRI for three months. Sequence-specific activation patterns emerged in the hippocampus during the first 1-2 weeks of learning, followed one week later by high-level visual cortex, and subsequently the medial prefrontal and parietal cortices. Schematic, sequence-general representations emerged in the prefrontal cortex after 3 weeks of learning, followed by the medial temporal lobe and anterior temporal cortex. Moreover, hippocampal and most neocortical representations showed sustained rather than time-limited dynamics, suggesting that representations tend to persist across learning. These results show that specific hippocampal representations emerge early, followed by both specific and schematic representations at a gradient of timescales across hippocampal-cortical networks as learning unfolds. Thus, memory representations do not exist only in specific brain regions at a given point in time, but are simultaneously present at multiple levels of abstraction across hippocampal-cortical networks.

Long-term learning transforms prefrontal cortex representations during working memory.

The role of the lateral prefrontal cortex (lPFC) in working memory (WM) is debated. Non-human primate (NHP) electrophysiology shows that the lPFC stores WM representations, but human neuroimaging suggests that the lPFC controls WM content in sensory cortices. These accounts are confounded by differences in task training and stimulus exposure. We tested whether long-term training alters lPFC function by densely sampling WM activity using functional MRI. Over 3 months, participants trained on both a WM and serial reaction time (SRT) task, wherein fractal stimuli were embedded within sequences. WM performance improved for trained (but not novel) fractals and, neurally, delay activity increased in distributed lPFC voxels across learning. Item-level WM representations became detectable within lPFC patterns, and lPFC activity reflected sequence relationships from the SRT task. These findings demonstrate that human lPFC develops stimulus-selective responses with learning, and WM representations are shaped by long-term experience, which could reconcile competing accounts of WM functioning.

Hemisphere-specific Parietal Contributions to the Interplay between Working Memory and Attention.

To achieve our moment-to-moment goals, we must often keep information temporarily in mind. Yet, this working memory (WM) may compete with demands for our attention in the environment. Attentional and WM functions are thought to operate by similar underlying principles, and they often engage overlapping fronto-parietal brain regions. In a recent fMRI study, bilateral parietal cortex BOLD activity displayed an interaction between WM and visual attention dual-task demands. However, prior studies also suggest that left and right parietal cortices make unique contributions to WM and attentional functions. Moreover, behavioral performance often shows no interaction between concurrent WM and attentional demands. Thus, the scope of reciprocity between WM and attentional functions, as well as the specific contribution that parietal cortex makes to these functions, remain unresolved. Here, we took a causal approach, targeting brain regions that are implicated in shared processing between WM and visual attention, to better characterize how those regions contribute to behavior. We first examined whether behavioral indices of WM and visual search differentially correlate with left and right parietal dual-task BOLD responses. Then, we delivered TMS over fMRI-guided left and right parietal sites during dual-task WM-visual search performance. Only right-parietal TMS influenced visual search behavior, but the stimulation either helped or harmed search depending on the current WM load. Therefore, whereas the left and right parietal contributions were distinct here, attentional and WM functions were codependent. Right parietal cortex seems to hold a privileged role in visual search behavior, consistent with prior findings, but the current results reveal that behavior may be sensitive to the interaction between visual search and WM load only when normal parietal activity is perturbed. The parietal response to heightened WM and attentional demands may therefore serve to protect against dual-task interference.

Prioritized verbal working memory content biases ongoing action.

Working memory (WM) holds information temporarily in mind, imparting the ability to guide behavior based on internal goals rather than external stimuli. However, humans often maintain WM content for a future task while performing more immediate actions. Consequently, transient WM representations may inadvertently influence ongoing (but unrelated) motor behavior. Here, we tested the impact of WM on adult human action execution and examined how the attentional or "activation" state of WM content modulates that impact. In 3 dual-task experiments, verbal WM for directional words influenced the trajectory and speed of hand movements performed during WM maintenance. This movement bias was also modulated by the attentional state of the WM content. Prioritized WM content strongly influenced actions during WM maintenance, while de-prioritized WM content was less influential. In summary, WM can unintentionally shape ongoing motor behavior, but the behavioral relevance of WM content determines the degree of influence on motor output. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

We Need a Taxonomy of Working Memory.

A vast and diverse literature describes the relationship between working memory and attention. That literature encompasses tests of the interactions between the two functions, comparisons of the processes underlying them, and theoretical formulations of the cognitive constructs. In a recent review, Oberauer (2019) reins in this varied work to create a roadmap for future research. Here, I delineate several additional considerations to guide the evaluation and development of research into working memory and attention. Namely, working memory is a complex construct that can entail many processes and take on several meanings. Research and theory about working memory-and its relation to attention-must consider what particular demands are being tapped, what type of information is being operated on, and what goal is ultimately at stake.

Practical Considerations for Navigating Registered Reports.

Recent open science efforts to improve rigor and reliability have sparked great enthusiasm. Among these, the Registered Report publication format integrates best practices in hypothesis-driven research with peer review that occurs before the research is conducted. Here, we detail practical recommendations to help researchers negotiate the mechanics of this developing format.

Neural Representation of Working Memory Content Is Modulated by Visual Attentional Demand.

Recent theories assert that visual working memory (WM) relies on the same attentional resources and sensory substrates as visual attention to external stimuli. Behavioral studies have observed competitive tradeoffs between internal (i.e., WM) and external (i.e., visual) attentional demands, and neuroimaging studies have revealed representations of WM content as distributed patterns of activity within the same cortical regions engaged by perception of that content. Although a key function of WM is to protect memoranda from competing input, it remains unknown how neural representations of WM content are impacted by incoming sensory stimuli and concurrent attentional demands. Here, we investigated how neural evidence for WM information is affected when attention is occupied by visual search-at varying levels of difficulty-during the delay interval of a WM match-to-sample task. Behavioral and fMRI analyses suggested that WM maintenance was impacted by the difficulty of a concurrent visual task. Critically, multivariate classification analyses of category-specific ventral visual areas revealed a reduction in decodable WM-related information when attention was diverted to a visual search task, especially when the search was more difficult. This study suggests that the amount of available attention during WM maintenance influences the detection of sensory WM representations.

Serial Dependence across Perception, Attention, and Memory.

Information that has been recently perceived or remembered can bias current processing. This has been viewed as both a corrupting (e.g., proactive interference in short-term memory) and stabilizing (e.g., serial dependence in perception) phenomenon. We hypothesize that this bias is a generally adaptive aspect of brain function that leads to occasionally maladaptive outcomes.

Reduced Risk-Taking following Disruption of the Intraparietal Sulcus.

Decision makers frequently encounter opportunities to pursue great gains-assuming they are willing to accept greater risks. Previous neuroimaging studies have shown that activity in the intraparietal sulcus (IPS) and the inferior frontal junction (IFJ) are associated with individual preferences for economic risk ("known unknowns," e.g., a 50% chance of winning $5) and ambiguity ("unknown unknowns," e.g., an unknown chance of winning $5), respectively. Whether processing in these regions causally enables risk-taking for individual decisions, however, remains unknown. To examine this question, we assessed the decision to engage in risk-taking after disrupting neural processing in the IPS and IFJ of healthy human participants using repetitive transcranial magnetic stimulation. While stimulation of the IFJ resulted in general slowing of decision times, disrupting neural processing within the IPS selectively suppressed risk-taking, biasing choices toward certain options featuring both lower risks and lower expected rewards. Our results are the first to demonstrate the necessity of intact IPS function for choosing uncertain outcomes when faced with calculable risks and rewards. Engagement of IPS during decision making may support a willingness to accept uncertain outcomes for a chance to obtain greater gains.

Center-Surround Inhibition in Working Memory.

Directing visual attention toward a particular feature or location in the environment suppresses processing of nearby stimuli [1-4]. Echoing the center-surround organization of retinal ganglion cell receptive fields [5], and biasing of competitive local neuronal dynamics in favor of task-relevant stimuli [6], this "inhibitory surround" attention mechanism accentuates the demarcation between task-relevant and irrelevant items. Here, we show that internally maintaining a color stimulus in working memory (WM), rather than visually attending the stimulus in the external environment, produces an analogous pattern of inhibition for stimuli that are nearby in color space. Replicating a well-known effect of attentional capture by stimuli that match WM content [7], visual attention was biased toward (task-irrelevant) stimuli that exactly matched a WM item. This bias was curtailed, however, for stimuli that were very similar to the WM content (i.e., within the inhibitory zone surrounding the focus of WM) and recovered for less similar stimuli (i.e., beyond the bounds of the inhibitory surround). Moreover, the expression of this inhibition effect was positively associated with WM performance across observers. In a second experiment, inhibition also occurred between two similar items simultaneously held in WM. This suggests that maintenance in WM is characterized by an excitatory peak centered on the focus of (internal) attention, surrounded by an inhibitory zone to limit interference by irrelevant and confusable representations. Here, thus, we show for the first time that the same center-surround selection mechanism that focuses visual attention on sensory stimuli also selectively maintains internally activated representations in WM.

Attentional guidance by working memory differs by paradigm: an individual-differences approach.

The contents of working memory (WM) have been repeatedly found to guide the allocation of visual attention; in a dual-task paradigm that combines WM and visual search, actively holding an item in WM biases visual attention towards memory-matching items during search (e.g., Soto et al., Journal of Experimental Psychology: Human Perception and Performance, 31(2), 248-261, 2005). A key debate is whether such memory-based attentional guidance is automatic or under strategic control. Generally, two distinct task paradigms have been employed to assess memory-based guidance, one demonstrating that attention is involuntarily captured by memory-matching stimuli even at a cost to search performance (Soto et al., 2005), and one demonstrating that participants can strategically avoid memory-matching distractors to facilitate search performance (Woodman & Luck, Journal of Experimental Psychology: Human Perception and Performance, 33(2), 363-377, 2007). The current study utilized an individual-differences approach to examine why the different paradigms--which presumably tap into the same attentional construct--might support contrasting interpretations. Participants completed a battery of cognitive tasks, including two types of attentional guidance paradigms (see Soto et al., 2005; Woodman & Luck, 2007), a visual WM task, and an operation span task, as well as attention-related self-report assessments. Performance on the two attentional guidance paradigms did not correlate. Subsequent exploratory regression analyses revealed that memory-based guidance in each task was differentially predicted by visual WM capacity for one paradigm, and by attention-related assessment scores for the other paradigm. The current results suggest that these two paradigms--which have previously produced contrasting patterns of performance--may probe distinct aspects of attentional guidance.

Resource-sharing between internal maintenance and external selection modulates attentional capture by working memory content.

It is unclear why and under what circumstances working memory (WM) and attention interact. Here, we apply the logic of the time-based resource-sharing (TBRS) model of WM (e.g., Barrouillet et al., 2004) to explore the mixed findings of a separate, but related, literature that studies the guidance of visual attention by WM contents. Specifically, we hypothesize that the linkage between WM representations and visual attention is governed by a time-shared cognitive resource that alternately refreshes internal (WM) and selects external (visual attention) information. If this were the case, WM content should guide visual attention (involuntarily), but only when there is time for it to be refreshed in an internal focus of attention. To provide an initial test for this hypothesis, we examined whether the amount of unoccupied time during a WM delay could impact the magnitude of attentional capture by WM contents. Participants were presented with a series of visual search trials while they maintained a WM cue for a delayed-recognition test. WM cues could coincide with the search target, a distracter, or neither. We varied both the number of searches to be performed, and the amount of available time to perform them. Slowing of visual search by a WM matching distracter-and facilitation by a matching target-were curtailed when the delay was filled with fast-paced (refreshing-preventing) search trials, as was subsequent memory probe accuracy. WM content may, therefore, only capture visual attention when it can be refreshed, suggesting that internal (WM) and external attention demands reciprocally impact one another because they share a limited resource. The TBRS rationale can thus be applied in a novel context to explain why WM contents capture attention, and under what conditions that effect should be observed.

The working memory stroop effect: when internal representations clash with external stimuli.

Working memory (WM) has recently been described as internally directed attention, which implies that WM content should affect behavior exactly like an externally perceived and attended stimulus. We tested whether holding a color word in WM, rather than attending to it in the external environment, can produce interference in a color-discrimination task, which would mimic the classic Stroop effect. Over three experiments, the WM Stroop effect recapitulated core properties of the classic attentional Stroop effect, displaying equivalent congruency effects, additive contributions from stimulus- and response-level congruency, and susceptibility to modulation by the percentage of congruent and incongruent trials. Moreover, WM maintenance was inversely related to attentional demands during the WM delay between stimulus presentation and recall, with poorer memory performance following incongruent than congruent trials. Together, these results suggest that WM and attention rely on the same resources and operate over the same representations.

Dissociable causal roles for left and right parietal cortex in controlling attentional biases from the contents of working memory.

The contents of working memory (WM) steer visual attention, but the extent of this guidance can be strategically enhanced or inhibited when WM content is reliably helpful or harmful to a visual task. Current understanding of the neural substrates mediating the cognitive control over WM biases is limited, however, by the correlational nature of functional MRI approaches. A recent fMRI study provided suggestive evidence for a functional lateralization of these control processes in posterior parietal cortex (PPC): activity in left PPC correlated with the presentation of WM cues that ought to be strategically enhanced to optimize performance, while activity in the right PPC correlated with the presentation of cues that ought to be inhibited to prevent detrimental attentional biases in a visual search. Here, we aimed to directly assess whether the left and right PPC are causally involved in the cognitive control of WM biases, and to clarify their precise functional contributions. We therefore applied 1 Hz repetitive transcranial magnetic stimulation (rTMS) to left and right PPC (and a vertex control site) prior to administering a behavioral task assessing WM biasing control functions. We observed that the perturbation of left PPC eliminated the strategic benefit of predictably helpful WM cueing, while the perturbation of right PPC amplified the cost of unpredictable detrimental WM cueing. The left and right PPC thus play distinct causal roles in WM-attention interactions: the left PPC to maximize benefits, and the right PPC to minimize costs, of internally maintained content on visual attention.

Working memory as internal attention: toward an integrative account of internal and external selection processes.

Working memory (WM) and attention have been studied as separate cognitive constructs, although it has long been acknowledged that attention plays an important role in controlling the activation, maintenance, and manipulation of representations in WM. WM has, conversely, been thought of as a means of maintaining representations to voluntarily guide perceptual selective attention. It has more recently been observed, however, that the contents of WM can capture visual attention, even when such internally maintained representations are irrelevant, and often disruptive, to the immediate external task. Thus, the precise relationship between WM and attention remains unclear, but it appears that they may bidirectionally impact one another, whether or not internal representations are consistent with the external perceptual goals. This reciprocal relationship seems, further, to be constrained by limited cognitive resources to handle demands in either maintenance or selection. We propose here that the close relationship between WM and attention may be best described as a give-and-take interdependence between attention directed toward either actively maintained internal representations (traditionally considered WM) or external perceptual stimuli (traditionally considered selective attention), underpinned by their shared reliance on a common cognitive resource. Put simply, we argue that WM and attention should no longer be considered as separate systems or concepts, but as competing and influencing one another because they rely on the same limited resource. This framework can offer an explanation for the capture of visual attention by irrelevant WM contents, as well as a straightforward account of the underspecified relationship between WM and attention.

A parieto-medial temporal pathway for the strategic control over working memory biases in human visual attention.

The contents of working memory (WM) can both aid and disrupt the goal-directed allocation of visual attention. WM benefits attention when its contents overlap with goal-relevant stimulus features, but WM leads attention astray when its contents match features of currently irrelevant stimuli. Recent behavioral data have documented that WM biases of attention may be subject to strategic cognitive control processes whereby subjects are able to either enhance or inhibit the influence of WM contents on attention. However, the neural mechanisms supporting cognitive control over WM biases on attention are presently unknown. Here, we characterize these mechanisms by combining human functional magnetic resonance imaging with a task that independently manipulates the relationship between WM cues and attention targets during visual search (with WM contents matching either search targets or distracters), as well as the predictability of this relationship (100 vs 50% predictability) to assess participants' ability to strategically enhance or inhibit WM biases on attention when WM contents reliably matched targets or distracter stimuli, respectively. We show that cues signaling predictable (> unpredictable) WM-attention relations reliably enhanced search performance, and that this strategic modulation of the interplay between WM contents and visual attention was mediated by a neuroanatomical network involving the posterior parietal cortex, the posterior cingulate, and medial temporal lobe structures, with responses in the hippocampus proper correlating with behavioral measures of strategic control of WM biases. Thus, we delineate a novel parieto-medial temporal pathway implementing cognitive control over WM biases to optimize goal-directed selection.

Cognitive control over working memory biases of selection.

Across many studies, researchers have found that representations in working memory (WM) can guide visual attention toward items that match the features of the WM contents. While some researchers have contended that this occurs involuntarily, others have suggested that the impact of WM contents on attention can be strategically controlled. Here, we varied the probability that WM items would coincide with either targets or distractors in a visual search task to examine (1) whether participants could intentionally enhance or inhibit the influence of WM items on attention and (2) whether cognitive control over WM biases would also affect access to the memory contents in a surprise recognition test. We found visual search to be faster when the WM item coincided with the search target, and this effect was enhanced when the memory item reliably predicted the location of the target. Conversely, visual search was slowed when the memory item coincided with a search distractor, and this effect was diminished, but not abolished, when the memory item was reliably associated with distractors. This strategic dampening of the influence of WM items on attention came at a price to memory, however, as participants were slowest to perform WM recognition tests on blocks in which the WM contents were consistently invalid. These results document that attentional capture by WM contents is partly, but not fully, malleable by top-down control, which appears to adjust the state of the WM contents to optimize search behavior. These data illustrate the role of cognitive control in modulating the strength of WM biases of selection, and they support a tight coupling between WM and attention.

The influence of concentrative meditation training on the development of attention networks during early adolescence.

We investigate if concentrative meditation training (CMT) offered during adolescent development benefits subsystems of attention using a quasi-experimental design. Attentional alerting, orienting, and conflict monitoring were examined using the Attention Network Test (ANT) in 13-15 year old children who received CMT as part of their school curriculum (CMT group: N = 79) vs. those who received no such training (control group: N = 76). Alerting and conflict monitoring, but not orienting, differed between the CMT and control group. Only conflict monitoring demonstrated age-related improvements, with smaller conflict effect scores in older vs. younger participants. The influence of CMT on this system was similar to the influence of developmental maturity, with smaller conflict effects in the CMT vs. control group. To examine if CMT might also bolster conflict-triggered upregulation of attentional control, conflict effects were evaluated as a function of previous trial conflict demands (high conflict vs. low conflict). Smaller current-trial conflict effects were observed when previous conflict was high vs. low, suggesting that similar to adults, when previous conflict was high (vs. low) children in this age-range proactively upregulated control so that subsequent trial performance was benefitted. The magnitude of conflict-triggered control upregulation was not bolstered by CMT but CMT did have an effect for current incongruent trials preceded by congruent trials. Thus, CMT's influence on attention may be tractable and specific; it may bolster attentional alerting, conflict monitoring and reactive control, but does not appear to improve orienting.

Working-memory-triggered dynamic adjustments in cognitive control.

Dynamic adjustments in cognitive control are well documented in conflict tasks, wherein competition from irrelevant stimulus attributes intensifies selection demands and leads to subsequent performance benefits. The current study investigated whether mnemonic demands, in a working memory (WM) task, can drive similar online control modifications. Demand levels (high vs. low) of WM maintenance (memory load of 2 items vs. 1 item) and delay-spanning distractor interference (confusable vs. not confusable with memoranda) were manipulated using a factorial design during a WM delayed-recognition task. Performance was best subsequent to trials in which both maintenance and distractor interference demands were high, followed by trials with high demand in either of these 2 control domains, and worst following trials with low demand in both domains. These results suggest that dynamic adjustments in cognitive control are not triggered exclusively by conflict-specific contexts but are also triggered by WM demands, revealing a putative mechanism by which this system configures itself for successful task performance.