Valerie M. Beck

Reduced capacity but spared precision and maintenance of working memory representations in schizophrenia

CONTEXT Working memory deficits are considered a core feature of schizophrenia. Several recent integrative articles have offered mechanistic computational and neurobiological models of the origins of this cognitive deficit. OBJECTIVE To test predictions of these models using a new experimental paradigm from the basic science literature that makes it possible to determine whether patients with schizophrenia show (1) deficits in working memory storage capacity, (2) deficits in the precision of working memory representations, and (3) an amplification of these deficits as the retention interval increases. DESIGN Case-control design. All subjects performed a color working memory test in which they were asked to recall 3 or 4 items after a 1- or 4-second delay. All subjects also received a standard measure of intelligence and the Matrics Consensus Cognitive Battery. SETTING A tertiary care research outpatient clinic. Patients A total of 31 clinically stable patients with a DSM-IV diagnosis of schizophrenia or schizoaffective disorder and 26 healthy volunteers participated. The 2 groups were similar in age, sex, and ethnicity distribution. MAIN OUTCOME MEASURES (1) The number of items stored in working memory and (2) the precision of the working memory representations. RESULTS Patients showed a clear reduction in the number of items stored in working memory. Patients did not differ from controls in the precision of their working memory representations. There was no evidence of delay-related amplification of impairment in either capacity or precision. CONCLUSIONS Patients do not show the type of imprecision or delay-dependent amplification of impairment that is predicted on the basis of current models of the neurobiology of schizophrenia. The models need to be revised to account for a pure reduction in the number of items that patients are able to store in working memory.

Failure of schizophrenia patients to overcome salient distractors during working memory encoding.

BACKGROUND Prior demonstrations of impaired attentional control in schizophrenia focused on conditions in which top-down control is needed to overcome prepotent response tendencies. Attentional control over stimulus processing has received little investigation. Here, we test whether attentional control is impaired during working memory encoding when salient distractors compete with less salient task-relevant stimuli. METHODS Patients with schizophrenia (n = 28) and healthy control subjects (n = 25) performed a visuospatial working memory paradigm in which half of the to-be-encoded stimuli flickered to increase their salience. After a 2-second delay, stimuli reappeared and participants had to decide whether or not a probed item had shifted location. RESULTS In the unbiased condition where flickering and nonflickering stimuli were equally likely to be probed, both groups displayed a trend toward better memory for the flickering items. In the flicker-bias condition in which the flickering stimuli were likely to be probed, both groups displayed a robust selection advantage for the flickering items. However, in the nonflicker-bias condition in which the nonflickering stimuli were likely to be probed, only healthy control subjects showed selection of the nonflickering items. Patients displayed a trend toward preferential memory for the flickering items, as in the unbiased condition. CONCLUSIONS Both groups were able to select salient over nonsalient stimuli, but patients with schizophrenia were unable to select nonsalient over salient stimuli, consistent with impairment in the effortful control of attention. These findings demonstrate the generality of top-down control failure in schizophrenia in the face of bottom-up competition from salient stimuli as with prepotent response tendencies.

Control of working memory content in schizophrenia

People with schizophrenia (PSZ) exhibit signs of reduced working memory (WM) capacity. However, this may reflect an impairment in managing its content, e.g. preventing irrelevant information from taking up available storage space, rather than a true capacity reduction. We tested the ability to eliminate and update WM content in 38 PSZ and 30 healthy control subjects (HCS). Images of real-world objects were presented consecutively, and a tone cued the item most likely to be tested for memory. On half the trials, randomly intermixed, a second tone occurred. Participants were informed that the item cued by the second tone was now the most likely to be tested, and the item cued by the first tone now the least likely, providing incentive to eliminate the first cued item from WM. Both HCS and PSZ displayed a robust performance advantage for cued items. Unexpectedly, PSZ more efficiently removed the no-longer-essential item from WM than HCS. The magnitude of the WM clearance of this first cued item correlated with memory performance for the newly prioritized second cued item in PSZ, indicating that it was adaptive. However, WM clearance was not associated with WM capacity, ruling out the need to budget limited resources as an explanation for greater clearance in PSZ. A robust correlation between WM clearance and poverty of speech in PSZ instead suggests that the propensity to rapidly clear non-essential information and minimize the number of items in WM may be the reflection of a negative symptom trait. This finding may reflect a more general tendency of PSZ to focus processing more narrowly than HCS.

Evidence for negative feature guidance in visual search is explained by spatial recoding.

Theories of attention and visual search explain how attention is guided toward objects with known target features. But can attention be directed away from objects with a feature known to be associated only with distractors? Most studies have found that the demand to maintain the to-be-avoided feature in visual working memory biases attention toward matching objects rather than away from them. In contrast, Arita, Carlisle, and Woodman (2012) claimed that attention can be configured to selectively avoid objects that match a cued distractor color, and they reported evidence that this type of negative cue generates search benefits. However, the colors of the search array items in Arita et al. (2012) were segregated by hemifield (e.g., blue items on the left, red on the right), which allowed for a strategy of translating the feature-cue information into a simple spatial template (e.g., avoid right, or attend left). In the present study, we replicated the negative cue benefit using the Arita et al. (2012), method (albeit within a subset of participants who reliably used the color cues to guide attention). Then, we eliminated the benefit by using search arrays that could not be grouped by hemifield. Our results suggest that feature-guided avoidance is implemented only indirectly, in this case by translating feature-cue information into a spatial template.

Response activation impairments in schizophrenia: evidence from the lateralized readiness potential.

Previous research has demonstrated deficits in preresponse motor activity in schizophrenia, as evidenced by a reduced lateralized readiness potential (LRP). The LRP deficit could be due to increased activation of the incorrect response (e.g., failure to suppress competition) or to reduced activation of the correct response (e.g., a low-level impairment in response preparation). To distinguish these possibilities, we asked whether the LRP impairment is increased under conditions of strong response competition. We manipulated the compatibility of stimulus-response mappings (Experiment 1) and the compatibility of the target with flankers (Experiment 2). In both experiments, the patient LRP was reduced as much under conditions of low response competition as under high competition. These results are incompatible with a failure of patients to suppress competition and are instead consistent with a deficit in activating the correct response.

Memory-based attention capture when multiple items are maintained in visual working memory.

Efficient visual search requires that attention is guided strategically to relevant objects, and most theories of visual search implement this function by means of a target template maintained in visual working memory (VWM). However, there is currently debate over the architecture of VWM-based attentional guidance. We contrasted a single-item-template hypothesis with a multiple-item-template hypothesis, which differ in their claims about structural limits on the interaction between VWM representations and perceptual selection. Recent evidence from van Moorselaar, Theeuwes, and Olivers (2014) indicated that memory-based capture during search, an index of VWM guidance, is not observed when memory set size is increased beyond a single item, suggesting that multiple items in VWM do not guide attention. In the present study, we maximized the overlap between multiple colors held in VWM and the colors of distractors in a search array. Reliable capture was observed when 2 colors were held in VWM and both colors were present as distractors, using both the original van Moorselaar et al. singleton-shape search task and a search task that required focal attention to array elements (gap location in outline square stimuli). In the latter task, memory-based capture was consistent with the simultaneous guidance of attention by multiple VWM representations. (PsycINFO Database Record

Hyperfocusing in Schizophrenia: Evidence from Interactions Between Working Memory and Eye Movements

Recent research suggests that processing resources are focused more narrowly but more intensely in people with schizophrenia (PSZ) than in healthy control subjects (HCS), possibly reflecting local cortical circuit abnormalities. This hyperfocusing hypothesis leads to the counterintuitive prediction that, although PSZ cannot store as much information in working memory as HCS, the working memory representations that are present in PSZ may be more intense than those in HCS. To test this hypothesis, we used a task in which participants make a saccadic eye movement to a peripheral target and avoid a parafoveal nontarget while they are holding a color in working memory. Previous research with this task has shown that the parafoveal nontarget is more distracting when it matches the color being held in working memory. This effect should be enhanced in PSZ if their working memory representations are more intense. Consistent with this prediction, we found that the effect of a match between the distractor color and the memory color was larger in PSZ than in HCS. We also observed evidence that PSZ hyperfocused spatially on the region surrounding the fixation point. These results provide further evidence that some aspects of cognitive dysfunction in schizophrenia may be a result of a narrower and more intense focusing of processing resources.

Competition in saccade target selection reveals attentional guidance by simultaneously active working memory representations.

The content of visual working memory (VWM) guides attention, but whether this interaction is limited to a single VWM representation or functional for multiple VWM representations is under debate. To test this issue, we developed a gaze-contingent search paradigm to directly manipulate selection history and examine the competition between multiple cue-matching saccade target objects. Participants first saw a dual-color cue followed by two pairs of colored objects presented sequentially. For each pair, participants selectively fixated an object that matched one of the cued colors. Critically, for the second pair, the cued color from the first pair was presented either with a new distractor color or with the second cued color. In the latter case, if two cued colors in VWM interact with selection simultaneously, we expected the second cued color object to generate substantial competition for selection, even though the first cued color was used to guide attention in the immediately previous pair. Indeed, in the second pair, selection probability of the first cued color was substantially reduced in the presence of the second cued color. This competition between cue-matching objects provides strong evidence that both VWM representations interacted simultaneously with selection.

The architecture of interaction between visual working memory and visual attention.

In five experiments, we examined whether a task-irrelevant item in visual working memory (VWM) interacts with perceptual selection when VWM must also be used to maintain a template representation of a search target. This question is critical to distinguishing between competing theories specifying the architecture of interaction between VWM and attention. The single-item template hypothesis (SIT) posits that only a single item in VWM can be maintained in a state that interacts with attention. Thus, the secondary item should be inert with respect to attentional guidance. The multiple-item template hypothesis (MIT) posits that multiple items can be maintained in a state that interacts with attention; thus, both the target representation and the secondary item should be capable of guiding selection. This question has been addressed previously in attention capture studies, but the results have been ambiguous. Here, we modified these earlier paradigms to optimize sensitivity to capture. Capture by a distractor matching the secondary item in VWM was observed consistently across multiple types of search task (abstract arrays and natural scenes), multiple dependent measures (search reaction time (RT) and oculomotor capture), multiple memory dimensions (color and shape), and multiple search stimulus dimensions (color, shape, common objects), providing strong support for the MIT.

Whatever You Do, Don't Look at the ...: Evaluating Guidance by an Exclusionary Attentional Template

People can use a target template consisting of one or more features to guide attention and gaze to matching objects in a search array. But can we also use feature information to guide attention away from known irrelevant items? Some studies found a benefit from foreknowledge of a distractor feature, whereas others found a cost. Importantly, previous work has largely relied on end-of-trial manual responses; it is unclear how feature-guided avoidance might unfold as candidate objects are inspected. In the current experiments, participants were cued with a distractor feature to avoid, then performed a visual search task while eye movements were recorded. Participants initially fixated a to-be-avoided object more frequently than predicted by chance, but they also demonstrated avoidance of cue-matching objects later in the trial. When provided more time between cue stimulus and search array, participants continued to be initially captured by a cued-color item. Furthermore, avoidance of cue-matching objects later in the trial was not contingent on initial capture by a cue-matching object. These results suggest that the conflicting findings in previous negative-cue experiments may be explained by a mixture of two independent processes: initial attentional capture by memory-matching items and later avoidance of known irrelevant items.