Although areas of frontal cortex are thought to be critical for maintaining information in visuospatial working memory, the event-related potential (ERP) index of maintenance is found over posterior cortex in humans. In the present study, we reconcile these seemingly contradictory findings. Here we show that macaque monkeys and humans exhibit the same posterior ERP signature of working memory maintenance that predicts the precision of the memory-based behavioral responses. In addition, we show that the specific pattern of rhythmic oscillations in the alpha band, recently demonstrated to underlie the human visual working memory ERP component, is also present in monkeys. Next, we concurrently recorded intracranial local field potentials from two prefrontal and another frontal cortical area to determine their contribution to the surface potential indexing maintenance. The local fields in the two prefrontal areas, but not the cortex immediately posterior, exhibited amplitude modulations, timing, and relationships to behavior indicating that they contribute to the generation of the surface ERP component measured from the distal posterior electrodes. Rhythmic neural activity in the theta and gamma bands during maintenance provided converging support for the engagement of the same brain regions. These findings demonstrate that nonhuman primates have homologous electrophysiological signatures of visuospatial working memory to those of humans and that a distributed neural network, including frontal areas, underlies the posterior ERP index of visuospatial working memory maintenance.
In many theories of cognition, researchers propose that working memory and perception operate interactively. For example, in previous studies researchers have suggested that sensory inputs matching the contents of working memory will have an automatic advantage in the competition for processing resources. The authors tested this hypothesis by requiring observers to perform a visual search task while concurrently maintaining object representations in visual working memory. The hypothesis that working memory activation produces a simple but uncontrollable bias signal leads to the prediction that items matching the contents of working memory will automatically capture attention. However, no evidence for automatic attentional capture was obtained; instead, the participants avoided attending to these items. Thus, the contents of working memory can be used in a flexible manner for facilitation or inhibition of processing.
attention; working memory; visual search; capture
Theories of visual attention suggest that working memory representations automatically guide attention toward memory-matching objects. Some empirical tests of this prediction have produced results consistent with working memory automatically guiding attention. However, others have shown that individuals can strategically control whether working memory representations guide visual attention. Previous studies have not independently measured automatic and strategic contributions to the interactions between working memory and attention. In this study, we used a classic manipulation of the probability of valid, neutral, and invalid cues to tease apart the nature of such interactions. This framework utilizes measures of reaction time (RT) to quantify the costs and benefits of attending to memory-matching items and infer the relative magnitudes of automatic and strategic effects. We found both costs and benefits even when the memory-matching item was no more likely to be the target than other items, indicating an automatic component of attentional guidance. However, the costs and benefits essentially doubled as the probability of a trial with a valid cue increased from 20% to 80%, demonstrating a potent strategic effect. We also show that the instructions given to participants led to a significant change in guidance distinct from the actual probability of events during the experiment. Together, these findings demonstrate that the influence of working memory representations on attention is driven by both automatic and strategic interactions.
attention; working memory; cuing; automaticity; strategic control; PsychINFO classification 2346
The error-related negativity (ERN) and positivity (Pe) are components of event-related potential (ERP) waveforms recorded from humans that are thought to reflect performance monitoring. Error-related signals have also been found in single-neuron responses and local-field potentials recorded in supplementary eye field and anterior cingulate cortex of macaque monkeys. However, the homology of these neural signals across species remains controversial. Here, we show that monkeys exhibit ERN and Pe components when they commit errors during a saccadic stop-signal task. The voltage distributions and current densities of these components were similar to those found in humans performing the same task. Subsequent analyses show that neither stimulus- nor response-related artifacts accounted for the error-ERPs. This demonstration of macaque homologues of the ERN and Pe forms a keystone in the bridge linking human and nonhuman primate studies on the neural basis of performance monitoring.
Many recent studies of visual working memory have used change-detection tasks in which subjects view sequential displays and are asked to report whether they are identical or if one object has changed. A key question is whether the memory system used to perform this task is sufficiently flexible to detect changes in object identity independent of spatial transformations, but previous research has yielded contradictory results. To address this issue, the present study compared standard change-detection tasks with tasks in which the objects varied in size or position between successive arrays. Performance was nearly identical across the standard and transformed tasks unless the task implicitly encouraged spatial encoding. These results resolve the discrepancies in prior studies and demonstrate that the visual working memory system can detect changes in object identity across spatial transformations.
The effects of accessing or retrieving information held in working memory are poorly understood compared to what we know about the nature of information storage in this limited-capacity memory system. Previous studies of object-based attention have often relied upon memory-demanding tasks, and this work could indicate that accessing a piece of information in visual working memory may have deleterious effects upon the other representations being maintained. In the present study, we tested the hypothesis that accessing a feature of an object represented in visual working memory degrades the representations of the other stored objects’ features. Our findings support this hypothesis and point to important new questions about the nature of effects resulting from accessing information stored in visual working memory.
visual working memory; object-based attention; working memory access
Most theories of attention propose that we maintain attentional templates in visual working memory to control what information is selected. In the present study, we directly tested this proposal by measuring the contralateral-delay activity (CDA) of human event-related potentials (ERPs) during visual search tasks in which the target is cued on each trial. Here we show that the CDA can be used to measure the maintenance of attentional templates in visual working memory while processing complex visual scenes. In addition, this method allowed us to directly observe the shift from working memory to long-term memory representations controlling attention as learning occurred and experience accrued searching for the same target object. Our findings provide definitive support for several critical proposals made in theories of attention, learning, and automaticity.
To carry out tasks with the highest possible efficiency we have developed executive mechanisms which monitor task performance and optimize cognitive processing. It has been hypothesized that these executive mechanisms operate even without conscious awareness to maximize their sensitivity to task-relevant outcomes. To test this hypothesis the present study examined the error-related negativity (ERN), an electrophysiological index of the performance monitoring neural circuitry, during masked visual search. The findings show that representations of target objects that are processed perceptually but not to the level of awareness fail to elicit an ERN despite the ability of these targets to elicit a shift of attention. These findings indicate that the performance monitoring mechanism indexed by the ERN requires target information to be processed to the level of awareness for a mismatch between stimulus and response to be detected.
During the last decade one of the most contentious and heavily studied topics in the attention literature has been the role that working memory representations play in controlling perceptual selection. The hypothesis has been advanced that to have attention select a certain perceptual input from the environment, we only need to represent that item in working memory. Here we summarize the work indicating that the relationship between what representations are maintained in working memory and what perceptual inputs are selected is not so simple. First, it appears that attentional selection is also determined by high-level task goals that mediate the relationship between working memory storage and attentional selection. Second, much of the recent work from our laboratory has focused on the role of long-term memory in controlling attentional selection. We review recent evidence supporting the proposal that working memory representations are critical during the initial configuration of attentional control settings, but that after those settings are established long-term memory representations play an important role in controlling which perceptual inputs are selected by mechanisms of attention.
visual attention; visual working memory; long-term memory; event-related potentials
Symbolic visual cues indicating the location of an upcoming target are believed to invoke endogenous shifts of attention to cued locations. In the present study, we investigated how visual attention is shifted during such cuing paradigms by recording event-related potentials (ERPs). We focused on a component known to index lateralized shifts of perceptual attention during visual search tasks, known as the N2pc component. The ERP data show that attention was shifted to a cued location in anticipation of a target shape when the location is marked by a placeholder-object (Experiments 1 and 2). However, when the possible locations were not marked by placeholder objects we found no evidence for an anticipatory shift of attention to the cued location (Experiment 3). These findings indicate that the perceptual-attention mechanism indexed by the N2pc is deployed to objects and not simply locations in space devoid of object structure.
visual attention; attentional cuing; N2pc; event-related potentials; object-based attention
Indirect evidence suggests that the contents of visual working memory may be maintained within sensory areas early in the visual hierarchy. We tested this possibility using a well-studied motion repulsion phenomenon in which perception of one direction of motion is distorted when another direction of motion is viewed simultaneously. We found that observers misperceived the actual direction of motion of a single motion stimulus if, while viewing that stimulus, they were holding a different motion direction in visual working memory. Control experiments showed that none of a variety of alternative explanations could account for this repulsion effect induced by working memory. Our findings provide compelling evidence that visual working memory representations directly interact with the same neural mechanisms as those involved in processing basic sensory events.
Visual working memory; Visual perception
It has been intensely debated whether visual stimuli are processed to the point of semantic analysis in the absence of awareness. In the present study, we measured the extent to which the meaning of a stimulus was registered using the N400 component of human event-related potentials (ERPs), a highly sensitive index of the semantic mismatch between a stimulus and the context in which it is presented. Observers judged the semantic relatedness of a context and target word while ERPs were recorded under continuous flash suppression (Experiment 1 and 2) and binocular rivalry (Experiment 3). Finally, we parametrically manipulated the visibility of the target word by increasing the contrast between the target word and the suppressive stimulus presented to the other eye (Experiment 4). We found that the amplitude of the N400 was attenuated with increasing suppression depth and was absent whenever the observers could not discriminate the meaning of suppressed words. We discuss these findings in the context of single-process models of consciousness which can account for a large body of empirical evidence obtained from visual masking, attentional manipulations and, now, interocular suppression paradigms.
The role of spike rate versus timing codes in visual target selection is unclear. We simultaneously recorded activity from multiple frontal eye field neurons and asked whether they interacted to select targets from distractors during visual search. When both neurons in a pair selected the target and had overlapping receptive fields (RFs), they cooperated more than when one or neither neuron in the pair selected the target, measured by positive spike timing correlations using joint peristimulus time histogram analysis. The amount of cooperation depended on the location of the search target: it was higher when the target was inside both neurons’ RFs than when it was inside one RF but not the other, or outside both RFs. Elevated spike timing coincidences occurred at the time of attentional selection of the target as measured by average modulation of discharge rates. We observed competition among neurons with spatially non-overlapping RFs, measured by negative spike timing correlations. Thus, we provide evidence for dynamic and task-dependent cooperation and competition among frontal eye field neurons during visual target selection.
Attention; Saccade; Vision; Visual; Decision; Receptive Field; Redundancy; Macaque
The human visual system can notice differences between memories of previous visual inputs and perceptions of new visual inputs, but the comparison process that detects these differences has not been well characterized. This study tests the hypothesis that differences between the memory of a stimulus array and the perception of a new array are detected in a manner that is analogous to the detection of simple features in visual search tasks. That is, just as the presence of a task-relevant feature in visual search can be detected in parallel, triggering a rapid shift of attention to the object containing the feature, the presence of a memory-percept difference along a task-relevant dimension can be detected in parallel, triggering a rapid shift of attention to the changed object. Supporting evidence was obtained in a series of experiments that examined manual reaction times, saccadic reaction times, and event-related potential latencies. However, these experiments also demonstrated that a slow, limited-capacity process must occur before the observer can make a manual change-detection response.
Previous research suggests that target templates are stored visual working memory and used to guide attention during visual search. However, observers can search efficiently even if working memory is filled to capacity by a concurrent task. The idea that target templates are stored in working memory receives support primarily from studies of nonhuman primates in which the target varies from trial-to-trial, and it is possible that working memory templates are not necessary when target identity remains constant, as in most studies of visual search in humans. To test this hypothesis, we asked subjects to perform a visual search task during the delay interval of a visual working memory task. The two tasks were found to interfere with each other when the search targets changed from trial-to-trial, but not when target identity remained constant. Thus, a search template is stored in visual working memory only when the target varies from trial-to-trial. These findings suggest that the network of brain areas involved in shifting attention during visual search tasks may be able to operate essentially independently of the anatomical areas that perform visual working memory maintenance of objects, but only if the identity of the visual search target is stable across time.