Reassessing the Evidence for Capacity Limits in Neural Signals Related to Working Memory.

In 2004, two landmark studies described the discovery of brain imaging (functional magnetic resonance imaging and electroencephalography) signals that increase with the number of items held in visual working memory (WM). These studies claimed that the signals leveled off (plateaued) once the number of memoranda reached the capacity of WM, as estimated by the prevailing model of the time. However, alternative models were not considered, and changing concepts of WM in the more than a decade since these studies were published necessitate a re-evaluation of their findings; newer models that provide the most accurate account of behavioral data do not incorporate a fixed limit on the number of items stored. Furthermore, an important claim made about the original studies, that signals plateau at each individual's estimated capacity, has never been tested. Here, we pit the plateau model of signal strength against an alternative, saturation model, a biophysically plausible account in which signals increase continuously without plateau. We show that the saturation model provides a better description of the original data, challenging the assumption that imaging results provide evidence for a fixed item limit in WM

Evaluating and excluding swap errors in analogue tests of working memory.

When observers retrieve simple visual features from working memory, two kinds of error are typically confounded in their recall. First, responses reflect noise or variability within the feature dimension they were asked to report. Second, responses are corrupted by "swap errors", in which a different item from the memory set is reported in place of the one that was probed. Independent evaluation of these error sources is vital for understanding the structure of internal representations and their binding. However, previous methods for disentangling these errors have been critically dependent on assumptions about the noise distribution, which is a priori unknown. Here I address this question with novel non-parametric (NP) methods, which estimate swap frequency and feature variability with fewer prior assumptions, and without a fitting procedure. The results suggest that swap errors are considerably more prevalent than previously appreciated (accounting for more than a third of responses at set size 8). These methods also identify which items are swapped in for targets: when the target item is cued by location, the items in closest spatial proximity are most likely to be incorrectly reported, thus implicating noise in the probe feature dimension as a source of swap errors.This research was supported by the Wellcome Trust.This is the author accepted manuscript. It is currently embargoed pending publication

A neural model of retrospective attention in visual working memory.

An informative cue that directs attention to one of several items in working memory improves subsequent recall of that item. Here we examine the mechanism of this retro-cue effect using a model of short-term memory based on neural population coding. Our model describes recalled feature values as the output of an optimal decoding of spikes generated by a tuned population of neurons. This neural model provides a better account of human recall data than an influential model that assumes errors can be described as a mixture of normally distributed noise and random guesses. The retro-cue benefit is revealed to be consistent with a higher firing rate of the population encoding the cued versus uncued items, with no difference in tuning specificity. Additionally, a retro-cued item is less likely to be swapped with another item in memory, an effect that can also be explained by greater activity of the underlying population. These results provide a parsimonious account of the effects of retrospective attention on recall and demonstrate a principled method for investigating neural representations with behavioral tasks

No fixed item limit in visuospatial working memory.

Investigations of working memory capacity in the visual domain have converged on the concept of a limited supply of a representational medium, flexibly distributed between objects. Current debate centers on whether this medium is continuous, or quantized into 2 or 3 memory "slots". The latter model makes the strong prediction that, if an item in memory is probed, behavioral parameters will plateau when the number of items is the same or more than the number of slots. Here we examine short-term memory for object location using a two-dimensional pointing task. We show that recall variability for items in memory increases monotonically from 1 to 8 items. Using a novel method to isolate only those trials on which a participant correctly identifies the target, we show that response latency also increases monotonically from 1 to 8 items. We argue that both these findings are incompatible with a quantized model.Wellcome Trust (Grant ID: 106926)This is the final version of the article. It first appeared from Elsevier via http://dx.doi.org/10.1016/j.cortex.2016.07.02

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)

Visual Working Memory Is Independent of the Cortical Spacing Between Memoranda.

The sensory recruitment hypothesis states that visual short-term memory is maintained in the same visual cortical areas that initially encode a stimulus' features. Although it is well established that the distance between features in visual cortex determines their visibility, a limitation known as crowding, it is unknown whether short-term memory is similarly constrained by the cortical spacing of memory items. Here, we investigated whether the cortical spacing between sequentially presented memoranda affects the fidelity of memory in humans (of both sexes). In a first experiment, we varied cortical spacing by taking advantage of the log-scaling of visual cortex with eccentricity, presenting memoranda in peripheral vision sequentially along either the radial or tangential visual axis with respect to the fovea. In a second experiment, we presented memoranda sequentially either within or beyond the critical spacing of visual crowding, a distance within which visual features cannot be perceptually distinguished due to their nearby cortical representations. In both experiments and across multiple measures, we found strong evidence that the ability to maintain visual features in memory is unaffected by cortical spacing. These results indicate that the neural architecture underpinning working memory has properties inconsistent with the known behavior of sensory neurons in visual cortex. Instead, the dissociation between perceptual and memory representations supports a role of higher cortical areas such as posterior parietal or prefrontal regions or may involve an as yet unspecified mechanism in visual cortex in which stimulus features are bound to their temporal order.SIGNIFICANCE STATEMENT Although much is known about the resolution with which we can remember visual objects, the cortical representation of items held in short-term memory remains contentious. A popular hypothesis suggests that memory of visual features is maintained via the recruitment of the same neural architecture in sensory cortex that encodes stimuli. We investigated this claim by manipulating the spacing in visual cortex between sequentially presented memoranda such that some items shared cortical representations more than others while preventing perceptual interference between stimuli. We found clear evidence that short-term memory is independent of the intracortical spacing of memoranda, revealing a dissociation between perceptual and memory representations. Our data indicate that working memory relies on different neural mechanisms from sensory perception

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

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

Attenuation of Self-Generated Tactile Sensations Is Predictive, not Postdictive

When one finger touches the other, the resulting tactile sensation is perceived as weaker than the same stimulus externally imposed. This attenuation of sensation could result from a predictive process that subtracts the expected sensory consequences of the action, or from a postdictive process that alters the perception of sensations that are judged after the event to be self-generated. In this study we observe attenuation even when the fingers unexpectedly fail to make contact, supporting a predictive process. This predictive attenuation of self-generated sensation may have evolved to enhance the perception of sensations with an external cause

Competition between movement plans increases motor variability: evidence of a shared resource for movement planning.

Do movement plans, like representations in working memory, share a limited pool of resources? If so, the precision with which each individual movement plan is specified should decrease as the total number of movement plans increases. To explore this, human participants made speeded reaching movements toward visual targets. We examined if preparing one movement resulted in less variability than preparing two movements. The number of planned movements was manipulated in a delayed response cueing procedure that limited planning to a single target (experiment 1) or hand (experiment 2) or required planning of movements toward two targets (or with two hands). For both experiments, initial movement direction variability was higher in the two-plan condition than in the one-plan condition, demonstrating a cost associated with planning multiple movements, consistent with the limited resource hypothesis. In experiment 3, we showed that the advantage in initial variability of preparing a single movement was present only when the trajectory could be fully specified. This indicates that the difference in variability between one and two plans reflects the specification of full motor plans, not a general preparedness to move. The precision cost related to concurrent plans represents a novel constraint on motor preparation, indicating that multiple movements cannot be planned independently, even if they involve different limbs.This research was supported by the Wellcome Trust and the Van Coeverden Adriani Stichting.This is the author accepted manuscript. The final version is available from the American Physiological Society via http://dx.doi.org/10.1152/jn.00113.201