Representation and computation in visual working memory.

The ability to sustain internal representations of the sensory environment beyond immediate perception is a fundamental requirement of cognitive processing. In recent years, debates regarding the capacity and fidelity of the working memory (WM) system have advanced our understanding of the nature of these representations. In particular, there is growing recognition that WM representations are not merely imperfect copies of a perceived object or event. New experimental tools have revealed that observers possess richer information about the uncertainty in their memories and take advantage of environmental regularities to use limited memory resources optimally. Meanwhile, computational models of visuospatial WM formulated at different levels of implementation have converged on common principles relating capacity to variability and uncertainty. Here we review recent research on human WM from a computational perspective, including the neural mechanisms that support it.

A dynamic neural resource model bridges sensory and working memory.

Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or 'iconic' memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.

Neural tuning instantiates prior expectations in the human visual system.

Perception is often modelled as a process of active inference, whereby prior expectations are combined with noisy sensory measurements to estimate the structure of the world. This mathematical framework has proven critical to understanding perception, cognition, motor control, and social interaction. While theoretical work has shown how priors can be computed from environmental statistics, their neural instantiation could be realised through multiple competing encoding schemes. Using a data-driven approach, here we extract the brain's representation of visual orientation and compare this with simulations from different sensory coding schemes. We found that the tuning of the human visual system is highly conditional on stimulus-specific variations in a way that is not predicted by previous proposals. We further show that the adopted encoding scheme effectively embeds an environmental prior for natural image statistics within the sensory measurement, providing the functional architecture necessary for optimal inference in the earliest stages of cortical processing.

Role of time in binding features in visual working memory.

Previous research on feature binding in visual working memory has supported a privileged role for location in binding an object's nonspatial features. However, humans are able to correctly recall feature conjunctions of objects that occupy the same location at different times. In a series of behavioral experiments, we investigated binding errors under these conditions, and specifically tested whether ordinal position can take the role of location in mediating feature binding. We performed two dual report experiments in which participants had to memorize three colored shapes presented sequentially at the screen center. When participants were cued with the ordinal position of one item and had to report its shape and color, report errors for the two features were largely uncorrelated. In contrast, when participants were cued, for example, with an item's shape and reported an incorrect ordinal position, they had a high chance of making a corresponding error in the color report. This pattern of error correlations closely matched the predictions of a model in which color and shape are bound to each other only indirectly via an item's ordinal position. In a third experiment, we directly compared the roles of location and sequential position in feature binding. Participants viewed a sequence of colored disks displayed at different locations and were cued either by a disk's location or its ordinal position to report its remaining properties. The pattern of errors supported a mixed strategy with individual variation, suggesting that binding via either time or space could be used for this task. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Working memory is updated by reallocation of resources from obsolete to new items.

Visual working memory (VWM) resources are limited, placing constraints on how much visual information can be simultaneously retained. During visually guided activity, stored information can quickly become outdated, so updating mechanisms are needed to ensure the contents of memory remain relevant to current task goals. In particular, successful deallocation of resources from items that become obsolete is likely to be critical for maintaining the precision of those representations still in memory. The experiments in this study involved presenting two memory arrays of coloured disks in sequence. The appearance of the second array was a cue to replace, rehearse, or add a new colour to the colours in memory. We predicted that successful resource reallocation should result in comparable recall precision when an item was replaced or rehearsed, owing to the removal of pre-replacement features. In contrast, a failure to update WM should lead to comparable precision with a condition in which a new colour was added to memory. We identified a very small proportion (∼5%) of trials in which participants incorrectly reported a feature from the first array in place of its replacement in the second, which we interpreted as a failure to incorporate the information from the second display into memory. Once these trials were discounted, precision estimates were consistent with complete redistribution of resources in the case of updating a single item. We conclude that working memory can be efficiently updated when previous information becomes obsolete, but that this is a demanding active process that occasionally fails.

Perceptual similarity judgments do not predict the distribution of errors in working memory.

Population coding models provide a quantitative account of visual working memory (VWM) retrieval errors with a plausible link to the response characteristics of sensory neurons. Recent work has provided an important new perspective linking population coding to variables of signal detection, including d-prime, and put forward a new hypothesis: that the distribution of recall errors on, for example, a color wheel, is a consequence of the psychological similarity between points in that stimulus space, such that the exponential-like psychophysical distance scaling function can fulfil the role of population tuning and obviate the need to fit a tuning width parameter to recall data. Using four different visual feature spaces, we measured psychophysical similarity and memory errors in the same participants. Our results revealed strong evidence for a common source of variability affecting similarity judgments and recall estimates but did not support any consistent relationship between psychophysical similarity functions and VWM errors. At the group level, the responsiveness functions obtained from the psychophysical similarity task diverged strongly from those that provided the best fit to working memory errors. At the individual level, we found convincing evidence against an association between observed and best-fitting similarity functions. Finally, our results show that the newly proposed exponential-like responsiveness function has in general no advantage over the canonical von Mises (circular normal) function assumed by previous population coding models. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Swap errors in visual working memory are fully explained by cue-feature variability.

In cue-based recall from working memory, incorrectly reporting features of an uncued item may be referred to as a "swap" error. One account of these errors ascribes them to variability in memory for the cue features leading to erroneous selection of a non-target item, especially if it is similar to the target in the cue-feature dimension. However, alternative accounts of swap errors include cue-independent misbinding, and strategic guessing when the cued item is not in memory. Here we investigated the cause of swap errors by manipulating the variability with which either cue or report features (orientations in Exp 1; motion directions in Exp 2) were encoded. We found that swap errors increased with increasing variability in memory for the cue features, and their changing frequency could be quantitatively predicted based on recall variability when the same feature was used for report. These results are inconsistent with the hypothesis that swaps are a strategic response to forgotten items, and suggest that swap errors could be wholly accounted for by confusions due to cue-dimension variability. In a third experiment we examined whether spatial configuration of memory arrays in tasks with spatial cueing has an influence on swap error frequency. We observed a specific tendency to make swap errors to non-targets located precisely opposite to the cued location, suggesting that stimulus positions are partially encoded in a non-metric format.

Mechanisms of feature binding in visual working memory are stable over long delays.

The ability to accurately retain the binding between the features of different objects is a critical element of visual working memory. The underlying mechanism can be elucidated by analyzing correlations of response errors in dual-report experiments, in which participants have to report two features of a single item from a previously viewed stimulus array. Results from separate previous studies using different cueing conditions have indicated that location takes a privileged role in mediating binding between other features, in that largely independent response errors have been observed when location was used as a cue, but errors were highly correlated when location was one of the reported features. Earlier results from change detection tasks likewise support such a special role of location, but they also suggest that this role is substantially reduced for longer retention intervals in favor of object-based representation. In the present study, we replicated the findings of previous dual-report tasks with different cueing conditions, using matched stimuli and procedures. Moreover, we show that the observed patterns of error correlations remain qualitatively unchanged with longer retention intervals. Fits with neural population models demonstrate that the behavioral results at long, as well as short, delays are best explained by memory representations in independent feature maps, in which an item's features are bound to each other only via their shared location.

Transsaccadic integration operates independently in different feature dimensions.

Our knowledge about objects in our environment reflects an integration of current visual input with information from preceding gaze fixations. Such a mechanism may reduce uncertainty but requires the visual system to determine which information obtained in different fixations should be combined or kept separate. To investigate the basis of this decision, we conducted three experiments. Participants viewed a stimulus in their peripheral vision and then made a saccade that shifted the object into the opposite hemifield. During the saccade, the object underwent changes of varying magnitude in two feature dimensions (Experiment 1, color and location; Experiments 2 and 3, color and orientation). Participants reported whether they detected any change and estimated one of the postsaccadic features. Integration of presaccadic with postsaccadic input was observed as a bias in estimates toward the presaccadic feature value. In all experiments, presaccadic bias weakened as the magnitude of the transsaccadic change in the estimated feature increased. Changes in the other feature, despite having a similar probability of detection, had no effect on integration. Results were quantitatively captured by an observer model where the decision whether to integrate information from sequential fixations is made independently for each feature and coupled to awareness of a feature change.

Limited memory for ensemble statistics in visual change detection.

Accounts of working memory based on independent item representations may overlook a possible contribution of ensemble statistics, higher-order regularities of a scene such as the mean or variance of a visual attribute. Here we used change detection tasks to investigate the hypothesis that observers store ensemble statistics in working memory and use them to detect changes in the visual environment. We controlled changes to the ensemble mean or variance between memory and test displays across six experiments. We made specific predictions of observers' sensitivity using an optimal summation model that integrates evidence across separate items but does not detect changes in ensemble statistics. We found strong evidence that observers outperformed this model, but only when task difficulty was high, and only for changes in stimulus variance. Under these conditions, we estimated that the variance of items contributed to change detection sensitivity more strongly than any individual item in this case. In contrast, however, we found strong evidence against the hypothesis that the average feature value is stored in working memory: when the mean of memoranda changed, sensitivity did not differ from the optimal summation model, which was blind to the ensemble mean, in five out of six experiments. Our results reveal that change detection is primarily limited by uncertainty in the memory of individual features, but that memory for the variance of items can facilitate detection under a limited set of conditions that involve relatively high working memory demands.

Transsaccadic integration relies on a limited memory resource.

Saccadic eye movements cause large-scale transformations of the image falling on the retina. Rather than starting visual processing anew after each saccade, the visual system combines post-saccadic information with visual input from before the saccade. Crucially, the relative contribution of each source of information is weighted according to its precision, consistent with principles of optimal integration. We reasoned that, if pre-saccadic input is maintained in a resource-limited store, such as visual working memory, its precision will depend on the number of items stored, as well as their attentional priority. Observers estimated the color of stimuli that changed imperceptibly during a saccade, and we examined where reports fell on the continuum between pre- and post-saccadic values. Bias toward the post-saccadic color increased with the set size of the pre-saccadic display, consistent with an increased weighting of the post-saccadic input as precision of the pre-saccadic representation declined. In a second experiment, we investigated if transsaccadic memory resources are preferentially allocated to attentionally prioritized items. An arrow cue indicated one pre-saccadic item as more likely to be chosen for report. As predicted, valid cues increased response precision and biased responses toward the pre-saccadic color. We conclude that transsaccadic integration relies on a limited memory resource that is flexibly distributed between pre-saccadic stimuli.

Location-independent feature binding in visual working memory for sequentially presented objects.

Spatial location is believed to have a privileged role in binding features held in visual working memory. Supporting this view, Pertzov and Husain (Attention, Perception, & Psychophysics, 76(7), 1914-1924, 2014) reported that recall of bindings between visual features was selectively impaired when items were presented sequentially at the same location compared to sequentially at different locations. We replicated their experiment, but additionally tested whether the observed impairment could be explained by perceptual interference during encoding. Participants viewed four oriented bars in highly discriminable colors presented sequentially either at the same or different locations, and after a brief delay were cued with one color to reproduce the associated orientation. When we used the same timing as the original study, we reproduced its key finding of impaired binding memory in the same-location condition. Critically, however, this effect was significantly modulated by the duration of the inter-stimulus interval, and disappeared if memoranda were presented with longer delays between them. In a second experiment, we tested whether the effect generalized to other visual features, namely reporting of colors cued by stimulus shape. While we found performance deficits in the same-location condition, these did not selectively affect binding memory. We argue that the observed effects are best explained by encoding interference, and that memory for feature binding is not necessarily impaired when memoranda share the same location.

Consequence of stroke for feature recall and binding in visual working memory.

Visual memory for objects involves the integration, or binding, of individual features into a coherent representation. We used a novel approach to assess feature binding, using a delayed-reproduction task in combination with computational modeling and lesion analysis. We assessed stroke patients and neurotypical controls on a visual working memory task in which spatial arrays of colored disks were presented. After a brief delay, participants either had to report the color of one disk cued by its location or the location of one disk cued by its color. Our results demonstrate that, in the controls, report imprecision and swap errors (non-target reports) can be explained by a single source of variability. Stroke patients showed an overall decrease in memory precision for both color and location, with only limited evidence for deviations from the predicted relationship between report precision and swap errors. These deviations were primarily deficits in reporting items rather than selecting items based on the cue. Atlas-based lesion-symptom mapping showed that selection and reporting deficits, precision in reporting color, and precision in reporting location were associated with different lesion profiles. Deficits in binding are associated with lesions in the left somatosensory cortex, deficits in the precision of reporting color with bilateral fronto-parietal regions, and no anatomical substrates were identified for precision in reporting location. Our results converge with previous reports that working memory representations are widely distributed in the brain and can be found across sensory, parietal, temporal, and prefrontal cortices. Stroke patients demonstrate mostly subtle impairments in visual working memory, perhaps because representations from different areas in the brain can partly compensate for impaired encoding in lesioned areas. These findings contribute to understanding of the relation between memorizing features and their bound representations.

Stochastic sampling provides a unifying account of visual working memory limits.

Research into human working memory limits has been shaped by the competition between different formal models, with a central point of contention being whether internal representations are continuous or discrete. Here we describe a sampling approach derived from principles of neural coding as a framework to understand working memory limits. Reconceptualizing existing models in these terms reveals strong commonalities between seemingly opposing accounts, but also allows us to identify specific points of difference. We show that the discrete versus continuous nature of sampling is not critical to model fits, but that, instead, random variability in sample counts is the key to reproducing human performance in both single- and whole-report tasks. A probabilistic limit on the number of items successfully retrieved is an emergent property of stochastic sampling, requiring no explicit mechanism to enforce it. These findings resolve discrepancies between previous accounts and establish a unified computational framework for working memory that is compatible with neural principles.

Theory of neural coding predicts an upper bound on estimates of memory variability.

Observers reproducing elementary visual features from memory after a short delay produce errors consistent with the encoding-decoding properties of neural populations. While inspired by electrophysiological observations of sensory neurons in cortex, the population coding account of these errors is based on a mathematical idealization of neural response functions that abstracts away most of the heterogeneity and complexity of real neuronal populations. Here we examine a more physiologically grounded model based on the tuning of a large set of neurons recorded in macaque V1 and show that key predictions of the idealized model are preserved. Both models predict long-tailed distributions of error when memory resources are taxed, as observed empirically in behavioral experiments and commonly approximated with a mixture of normal and uniform error components. Specifically, for an idealized homogeneous neural population, the width of the fitted normal distribution cannot exceed the average tuning width of the component neurons, and this also holds to a good approximation for more biologically realistic populations. Examining eight published studies of orientation recall, we find a consistent pattern of results suggestive of a median tuning width of approximately 20°, which compares well with neurophysiological observations. The finding that estimates of variability obtained by the normal-plus-uniform mixture method are bounded from above leads us to reevaluate previous studies that interpreted a saturation in width of the normal component as evidence for fundamental limits on the precision of perception, working memory, and long-term memory. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

"The ipsilesional attention bias in right-hemisphere stroke patients as revealed by a realistic visual search task: Neuroanatomical correlates and functional relevance": Correction to Machner et al. (2018).

Reports an error in "The ipsilesional attention bias in right-hemisphere stroke patients as revealed by a realistic visual search task: Neuroanatomical correlates and functional relevance" by Björn Machner, Inga Könemund, Janina von der Gablentz, Paul M. Bays and Andreas Sprenger (Neuropsychology, 2018[Oct], Vol 32[7], 850-865). In the article, The copyright attribution was incorrectly listed and the Creative Commons CC-BY license disclaimer was incorrectly omitted from the author note. The correct copyright is "© 2018 The Author(s)" and the omitted disclaimer is below. The online version of this article has been corrected. "This article has been published under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Copyright for this article is retained by the author(s). Author(s) grant(s) the American Psychological Association the exclusive right to publish the article and identify itself as the original publisher." (The following abstract of the original article appeared in record 2018-51197-002.) Objective: Right-hemisphere stroke may cause an ipsilesional attention bias and left hemispatial neglect. Computerized time-limited tasks are more sensitive than conventional paper-pencil tests in detecting these spatial attention deficits. However, their frequency in the acute stage of stroke, the neuroanatomical basis and functional relevance for patients' everyday life are unclear. METHOD: A realistic visual search task is introduced, in which eye movements are recorded while the patient searches for paperclips among different everyday objects on a computer display. The "desk task" performance of 34 acute right-hemisphere stroke patients was compared to established paper-pencil tests for neglect and the Posner reaction time task, and finally correlated to structural brain lesions. RESULTS: Most of the patients, even those without clinical neglect signs and with normal paper-pencil test performance, exhibited a clear ipsilesional attention bias in the desk task. This bias was highly correlated to the left-right asymmetry in the Posner task and to neglect-related functional impairment scores. Lesion-symptom mapping revealed task-specific differences: deficits in the desk task were associated with lesions of the superior temporal gyrus, contralesional unawareness in the Posner task with ventral frontal cortex lesions and paper-pencil cancellation bias with damage to the inferior parietal lobe. Neglect behavior was further associated with distinct frontoparietal white matter tract disconnections (inferior longitudinal fasciculus, superior longitudinal fasciculus, arcuate). CONCLUSIONS: Results from the novel desk task indicate a functional relevance of spatial attention deficits in right-hemisphere stroke patients, even if they are "subclinical." This should be considered especially in patients without obvious clinical neglect signs. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

The effect of frontoparietal paired associative stimulation on decision-making and working memory.

Previous single-site neurostimulation experiments have unsuccessfully attempted to shift decision-making away from habitual control, a fast, inflexible cognitive strategy, towards goal-directed control, a flexible, though computationally expensive strategy. We employed a dual-target neurostimulation approach in 30 healthy participants, using cortico-cortical paired associative stimulation (ccPAS) to target two key nodes: lateral prefrontal cortex (LPFC) and intraparietal sulcus (IPS), to test whether decision-making can be artificially shifted from habitual toward goal-directed control. Participants received three active stimulations, delivered at least six days apart (each involving 100 paired pulses over the IPS and LPFC, varying the interstimulus interval): two interventional, time-relevant ccPAS (10 msec interval) and one control, non-time-relevant ccPAS (100 msec interval). Following stimulation, participants completed a sequential learning task, measuring goal-directed/habitual control, and a working memory task. IPS→LPFC ccPAS (stimulating IPS, then LPFC with a 10 msec interval) shifted decision-making from habitual toward goal-directed control, compared to control ccPAS. There was no effect of LPFC→IPS ccPAS, nor an effect of any PAS condition on working memory. Previous studies have shown ccPAS effects outside the motor domain targeting prefrontal regions on response inhibition, attentional bias, and alpha asymmetry. The present study measures the behavioural effects of parietal-prefrontal PAS, focusing on a highly complex decision-making task and working memory. If confirmed in larger studies, this would be the first instance of neurostimulation successfully shifting decision-making from habitual to goal-directed control, putatively via inducing long-term potentiation between the IPS and LPFC. However, we found no effect in the other direction (LPFC→IPS ccPAS), and no effect on working memory overall. PAS is a relatively new neuromodulatory technique in the cognitive arsenal, and this study could help guide future approaches in healthy and disordered decision-making.

Recall of facial expressions and simple orientations reveals competition for resources at multiple levels of the visual hierarchy.

Many studies of visual working memory have tested humans' ability to reproduce primary visual features of simple objects, such as the orientation of a grating or the hue of a color patch, following a delay. A consistent finding of such studies is that precision of responses declines as the number of items in memory increases. Here we compared visual working memory for primary features and high-level objects. We presented participants with memory arrays consisting of oriented gratings, facial expressions, or a mixture of both. Precision of reproduction for all facial expressions declined steadily as the memory load was increased from one to five faces. For primary features, this decline and the specific distributions of error observed, have been parsimoniously explained in terms of neural population codes. We adapted the population coding model for circular variables to the non-circular and bounded parameter space used for expression estimation. Total population activity was held constant according to the principle of normalization and the intensity of expression was decoded by drawing samples from the Bayesian posterior distribution. The model fit the data well, showing that principles of population coding can be applied to model memory representations at multiple levels of the visual hierarchy. When both gratings and faces had to be remembered, an asymmetry was observed. Increasing the number of faces decreased precision of orientation recall, but increasing the number of gratings did not affect recall of expression, suggesting that memorizing faces involves the automatic encoding of low-level features, in addition to higher-level expression information.

Independent working memory resources for egocentric and allocentric spatial information.

Visuospatial working memory enables us to maintain access to visual information for processing even when a stimulus is no longer present, due to occlusion, our own movements, or transience of the stimulus. Here we show that, when localizing remembered stimuli, the precision of spatial recall does not rely solely on memory for individual stimuli, but additionally depends on the relative distances between stimuli and visual landmarks in the surroundings. Across three separate experiments, we consistently observed a spatially selective improvement in the precision of recall for items located near a persistent landmark. While the results did not require that the landmark be visible throughout the memory delay period, it was essential that it was visible both during encoding and response. We present a simple model that can accurately capture human performance by considering relative (allocentric) spatial information as an independent localization estimate which degrades with distance and is optimally integrated with egocentric spatial information. Critically, allocentric information was encoded without cost to egocentric estimation, demonstrating independent storage of the two sources of information. Finally, when egocentric and allocentric estimates were put in conflict, the model successfully predicted the resulting localization errors. We suggest that the relative distance between stimuli represents an additional, independent spatial cue for memory recall. This cue information is likely to be critical for spatial localization in natural settings which contain an abundance of visual landmarks.