Nahid Zokaei

Precision of working memory for visual motion sequences and transparent motion surfaces

Recent studies investigating working memory for location, color, and orientation support a dynamic resource model. We examined whether this might also apply to motion, using random dot kinematograms (RDKs) presented sequentially or simultaneously. Mean precision for motion direction declined as sequence length increased, with precision being lower for earlier RDKs. Two alternative models of working memory were compared specifically to distinguish between the contributions of different sources of error that corrupt memory (W. Zhang & S. J. Luck, 2008 vs. P. M. Bays, R. F. G. Catalao, & M. Husain, 2009). The latter provided a significantly better fit for the data, revealing that decrease in memory precision for earlier items is explained by an increase in interference from other items in a sequence rather than random guessing or a temporal decay of information. Misbinding feature attributes is an important source of error in working memory. Precision of memory for motion direction decreased when two RDKs were presented simultaneously as transparent surfaces, compared to sequential RDKs. However, precision was enhanced when one motion surface was prioritized, demonstrating that selective attention can improve recall precision. These results are consistent with a resource model that can be used as a general conceptual framework for understanding working memory across a range of visual features.

The Role of Perceptual Load in Object Recognition

Predictions from perceptual load theory (Lavie, 19952005) regarding object recognition across the same or different viewpoints were tested. Results showed that high perceptual load reduces distracter recognition levels despite always presenting distracter objects from the same view. They also showed that the levels of distracter recognition were unaffected by a change in the distracter object view under conditions of low perceptual load. These results were found both with repetition priming measures of distracter recognition and with performance on a surprise recognition memory test. The results support load theory proposals that distracter recognition critically depends on the level of perceptual load. The implications for the role of attention in object recognition theories are discussed.

Visual short-term memory deficits associated with GBA mutation and Parkinson’s disease

Individuals with mutation in the lysosomal enzyme glucocerebrosidase (GBA) gene are at significantly high risk of developing Parkinson’s disease with cognitive deficit. We examined whether visual short-term memory impairments, long associated with patients with Parkinson’s disease, are also present in GBA-positive individuals—both with and without Parkinson’s disease. Precision of visual working memory was measured using a serial order task in which participants observed four bars, each of a different colour and orientation, presented sequentially at screen centre. Afterwards, they were asked to adjust a coloured probe bar’s orientation to match the orientation of the bar of the same colour in the sequence. An additional attentional ‘filtering’ condition tested patients’ ability to selectively encode one of the four bars while ignoring the others. A sensorimotor task using the same stimuli controlled for perceptual and motor factors. There was a significant deficit in memory precision in GBA-positive individuals—with or without Parkinson’s disease—as well as GBA-negative patients with Parkinson’s disease, compared to healthy controls. Worst recall was observed in GBA-positive cases with Parkinson’s disease. Although all groups were impaired in visual short-term memory, there was a double dissociation between sources of error associated with GBA mutation and Parkinson’s disease. The deficit observed in GBA-positive individuals, regardless of whether they had Parkinson’s disease, was explained by a systematic increase in interference from features of other items in memory: misbinding errors. In contrast, impairments in patients with Parkinson’s disease, regardless of GBA status, was explained by increased random responses. Individuals who were GBA-positive and also had Parkinson’s disease suffered from both types of error, demonstrating the worst performance. These findings provide evidence for dissociable signature deficits within the domain of visual short-term memory associated with GBA mutation and with Parkinson’s disease. Identification of the specific pattern of cognitive impairment in GBA mutation versus Parkinson’s disease is potentially important as it might help to identify individuals at risk of developing Parkinson’s disease.

Development of Visual Working Memory Precision in Childhood.

Visual working memory (VWM) is the facility to hold in mind visual information for brief periods of time. Developmental studies have suggested an increase during childhood in the maximum number of complete items that can simultaneously be stored in VWM. Here, we exploit a recent theoretical and empirical innovation to investigate instead the precision with which items are stored in VWM, where precision is a continuous measure reflecting VWM resolution. Ninety boys aged 7 to 13 years completed one-item and three-item VWM tasks in which stimuli were coloured bars varying in orientation. On each trial, participants used a rotating dial to reproduce the probed stimulus from memory. Results show linear age-related improvement in recall precision for both one-item and three-item VWM tasks. However, even the youngest age group stored a significant amount of information about all three items on the difficult 3-item VWM task. Importantly, the development of VWM precision was not accounted for by development on a sensorimotor control task. Whereas storage of a single complete item was previously thought to be well within the capacity limitations of the current age range, these results suggest protracted development during childhood and early adolescence in the resolution with which single and multiple items are stored in VWM. Probabilistic modelling of response distribution data suggests that improvement in VWM performance is attributable to a specific decrease in variability of stored feature representations, rather than to a decrease in misbinding or random noise. As such, we highlight a novel, potentially developmentally plausible mechanism that may underlie developmental improvement in VWM performance, independent of any alterations in the maximum number of complete items which can be stored.

Causal Evidence for a Privileged Working Memory State in Early Visual Cortex

Emerging evidence suggests that items held in working memory (WM) might not all be in the same representational state. One item might be privileged over others, making it more accessible and thereby recalled with greater precision. Here, using transcranial magnetic stimulation (TMS), we provide causal evidence in human participants that items in WM are differentially susceptible to disruptive TMS, depending on their state, determined either by task relevance or serial position. Across two experiments, we applied TMS to area MT+ during the WM retention of two motion directions. In Experiment 1, we used an “incidental cue” to bring one of the two targets into a privileged state. In Experiment 2, we presented the targets sequentially so that the last item was in a privileged state by virtue of recency. In both experiments, recall precision of motion direction was differentially affected by TMS, depending on the state of the memory target at the time of disruption. Privileged items were recalled with less precision, whereas nonprivileged items were recalled with higher precision. Thus, only the privileged item was susceptible to disruptive TMS over MT+. By contrast, precision of the nonprivileged item improved either directly because of facilitation by TMS or indirectly through reduced interference from the privileged item. Our results provide a unique line of evidence, as revealed by TMS over a posterior sensory brain region, for at least two different states of item representation in WM.

Flexibility of representational states in working memory.

The relationship between working memory (WM) and attention is a highly interdependent one, with evidence that attention determines the state in which items in WM are retained. Through focusing of attention, an item might be held in a more prioritized state, commonly termed as the focus of attention (FOA). The remaining items, although still retrievable, are considered to be in a different representational state. One means to bring an item into the FOA is to use retrospective cues (“retro-cues”) which direct attention to one of the objects retained in WM. Alternatively, an item can enter a privileged state once attention is directed towards it through bottom-up influences (e.g., recency effect) or by performing an action on one of the retained items (“incidental” cueing). In all these cases, the item in the FOA is recalled with better accuracy compared to the other items in WM. Far less is known about the nature of the other items in WM and whether they can be flexibly manipulated in and out of the FOA. We present data from three types of experiments as well as transcranial magnetic stimulation (TMS) to early visual cortex to manipulate the item inside FOA. Taken together, our results suggest that the context in which items are retained in WM matters. When an item remains behaviorally relevant, despite not being inside the FOA, re-focusing attention upon it can increase its recall precision. This suggests that a non-FOA item can be held in a state in which it can be later retrieved. However, if an item is rendered behaviorally unimportant because it is very unlikely to be probed, it cannot be brought back into the FOA, nor recalled with high precision. Under such conditions, some information appears to be irretrievably lost from WM. These findings, obtained from several different methods, demonstrate quite considerable flexibility with which items in WM can be represented depending upon context. They have important consequences for emerging state-dependent models of WM.

Visual short-term memory deficits in REM sleep behaviour disorder mirror those in Parkinson's disease

Individuals with REM sleep behaviour disorder (RBD) are at high risk of Parkinson’s disease. Rolinski, Zokaei et al. show that they also display the same pattern of visual short-term memory deficits as patients with Parkinson’s disease, and suggest that this ‘fingerprint’ of memory impairment could be a prodromal disease marker.

Attention is required for maintenance of feature binding in visual working memory

Working memory and attention are intimately connected. However, understanding the relationship between the two is challenging. Currently, there is an important controversy about whether objects in working memory are maintained automatically or require resources that are also deployed for visual or auditory attention. Here we investigated the effects of loading attention resources on precision of visual working memory, specifically on correct maintenance of feature-bound objects, using a dual-task paradigm. Participants were presented with a memory array and were asked to remember either direction of motion of random dot kinematograms of different colour, or orientation of coloured bars. During the maintenance period, they performed a secondary visual or auditory task, with varying levels of load. Following a retention period, they adjusted a coloured probe to match either the motion direction or orientation of stimuli with the same colour in the memory array. This allowed us to examine the effects of an attention-demanding task performed during maintenance on precision of recall on the concurrent working memory task. Systematic increase in attention load during maintenance resulted in a significant decrease in overall working memory performance. Changes in overall performance were specifically accompanied by an increase in feature misbinding errors: erroneous reporting of nontarget motion or orientation. Thus in trials where attention resources were taxed, participants were more likely to respond with nontarget values rather than simply making random responses. Our findings suggest that resources used during attention-demanding visual or auditory tasks also contribute to maintaining feature-bound representations in visual working memory—but not necessarily other aspects of working memory.

Cathodal transcranial direct current stimulation over posterior parietal cortex enhances distinct aspects of visual working memory

In this study, we investigated the effects of tDCS over the posterior parietal cortex (PPC) during a visual working memory (WM) task, which probes different sources of response error underlying the precision of WM recall. In two separate experiments, we demonstrated that tDCS enhanced WM precision when applied bilaterally over the PPC, independent of electrode configuration. In a third experiment, we demonstrated with unilateral electrode configuration over the right PPC, that only cathodal tDCS enhanced WM precision and only when baseline performance was low. Looking at the effects on underlying sources of error, we found that cathodal stimulation enhanced the probability of correct target response across all participants by reducing feature-misbinding. Only for low-baseline performers, cathodal stimulation also reduced variability of recall. We conclude that cathodal- but not anodal tDCS can improve WM precision by preventing feature-misbinding and hereby enhancing attentional selection. For low-baseline performers, cathodal tDCS also protects the memory trace. Furthermore, stimulation over bilateral PPC is more potent than unilateral cathodal tDCS in enhancing general WM precision.

Causes and consequences of limitations in visual working memory

Recent methodological and conceptual advances have led to a fundamental reappraisal of the nature of visual working memory (WM). A large corpus of evidence now suggests that there might not be a hard limit on the number of items that can be stored. Instead, WM may be better captured by a highly limited––but flexible––resource model. More resource can be allocated to prioritized items but, crucially, at a cost of reduced recall precision for other stored items. Expectations may modulate resource distribution, for example, through neural oscillations in the alpha band increasing inhibition of irrelevant cortical regions. Our understanding of the neural architecture of WM is also undergoing radical revision. Whereas the prefrontal cortex has previously dominated research endeavors, other cortical regions, such as early visual areas, are now considered to make an essential contribution, for example holding one or more items in a privileged state or “focus of attention” within WM. By contrast, the striatum is increasingly viewed as crucial in determining why and how items are gated into memory, while the hippocampus, it has controversially been argued, might be critical in the formation of temporally resilient conjunctions across features of stored items in WM.