Anastasia Kiyonaga

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.

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 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.

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.

Quality and accessibility of visual working memory during cognitive control of attentional guidance: A Bayesian model comparison approach

Working memory (WM) can guide visual attention toward memory-matching objects. This influence of WM on attention can be modulated by cognitive control, such that attentional guidance is strategically suppressed or enhanced depending on whether WM contents are reliably hurtful or helpful for the current task. Cognitive control over memory-based guidance has been hypothesized to operate via some modulation of the WM representation itself, but it is unclear whether this modulation affects representational quality (i.e., how precise is it?) or accessibility of WM content (i.e., how easily is it remembered or forgotten?). Using probabilistic model fitting and Bayesian model comparison techniques, we show that cognitive control over memory-based guidance impacts the probability of remembering, but not the precision of, items in WM. These findings suggest that the WM-attention interaction may depend on distinct functional states in WM, which are in turn characterized by how easily an item is remembered or forgotten.

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.

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.

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

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

5) and ambiguity (“unknown unknowns,” e.g., an unknown chance of winning

Competitive tradeoffs between working memory and attention: An fMRI approach

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.