The role of alpha oscillations in deriving and maintaining spatial relations in working memory.

Previous research has demonstrated distinct neural correlates for maintenance of abstract, relational versus concrete, sensory information in working memory (WM). Storage of spatial relations in WM results in suppression of posterior sensory regions, which suggests that sensory information is task-irrelevant when relational representations are maintained in WM. However, the neural mechanisms by which abstract representations are derived from sensory information remain unclear. Here, using electroencephalography, we investigated the role of alpha oscillations in deriving spatial relations from a sensory stimulus and maintaining them in WM. Participants encoded two locations into WM, then after an initial maintenance period, a cue indicated whether to convert the spatial information to another sensory representation or to a relational representation. Results revealed that alpha power increased over posterior electrodes when sensory information was converted to a relational representation, but not when the information was converted to another sensory representation. Further, alpha phase synchrony between posterior and frontal regions increased for relational compared to sensory trials during the maintenance period. These results demonstrate that maintaining spatial relations and locations in WM rely on distinct neural oscillatory patterns.

Lateralization in Alpha-Band Oscillations Predicts the Locus and Spatial Distribution of Attention.

Attending to a task-relevant location changes how neural activity oscillates in the alpha band (8-13Hz) in posterior visual cortical areas. However, a clear understanding of the relationships between top-down attention, changes in alpha oscillations in visual cortex, and attention performance are still poorly understood. Here, we tested the degree to which the posterior alpha power tracked the locus of attention, the distribution of attention, and how well the topography of alpha could predict the locus of attention. We recorded magnetoencephalographic (MEG) data while subjects performed an attention demanding visual discrimination task that dissociated the direction of attention from the direction of a saccade to indicate choice. On some trials, an endogenous cue predicted the target's location, while on others it contained no spatial information. When the target's location was cued, alpha power decreased in sensors over occipital cortex contralateral to the attended visual field. When the cue did not predict the target's location, alpha power again decreased in sensors over occipital cortex, but bilaterally, and increased in sensors over frontal cortex. Thus, the distribution and the topography of alpha reliably indicated the locus of covert attention. Together, these results suggest that alpha synchronization reflects changes in the excitability of populations of neurons whose receptive fields match the locus of attention. This is consistent with the hypothesis that alpha oscillations reflect the neural mechanisms by which top-down control of attention biases information processing and modulate the activity of neurons in visual cortex.

Maintenance of relational information in working memory leads to suppression of the sensory cortex.

Working memory (WM) for sensory-based information about individual objects and their locations appears to involve interactions between lateral prefrontal and sensory cortexes. The mechanisms and representations for maintenance of more abstract, nonsensory information in WM are unknown, particularly whether such actively maintained information can become independent of the sensory information from which it was derived. Previous studies of WM for individual visual items found increased electroencephalogram (EEG) alpha (8-13 Hz) power over posterior electrode sites, which appears to correspond to the suppression of cortical areas that represent irrelevant sensory information. Here, we recorded EEG while participants performed a visual WM task that involved maintaining either concrete spatial coordinates or abstract relational information. Maintenance of relational information resulted in higher alpha power in posterior electrodes. Furthermore, lateralization of alpha power due to a covert shift of attention to one visual hemifield was marginally weaker during storage of relational information than during storage of concrete information. These results suggest that abstract relational information is maintained in WM differently from concrete, sensory representations and that during maintenance of abstract information, posterior sensory regions become task irrelevant and are thus suppressed.

The search for the neural mechanisms of the set size effect.

The set size effect in visual search refers to the linear increase in response time (RT) or decrease in accuracy as the number of distractors increases. Previous human and monkey studies have reported a correlation between set size and neural activity in the frontal eye field (FEF) and intraparietal sulcus (IPS). In a recent functional magnetic resonance imaging study, we did not observe a set size effect in the superior precentral sulcus (sPCS, thought to be the human homolog of the FEF) and IPS in an oculomotor visual search task (Ikkai et al., 2011). Our task used placeholders in the search array, along with the target and distractors, in order to equate the amount of retinal stimulation for each set size. We here attempted to reconcile these differences with the results from a follow-up experiment in which the same oculomotor visual search task was used, but without placeholders. A strong behavioral set size effect was observed in both studies, with very similar saccadic RTs and slopes between RT and set size. However, a set size effect was now observed in the sPCS and IPS. We comment on this finding and discuss the role of these neural areas in visual search.

Common neural mechanisms supporting spatial working memory, attention and motor intention.

The prefrontal cortex (PFC) and posterior parietal cortex (PPC) are critical neural substrates for working memory. Neural activity persists in these regions during the maintenance of a working memory representation. Persistent activity, therefore, may be the neural mechanism by which information is temporarily maintained. However, the nature of the representation or what is actually being represented by this persistent activity is not well understood. In this review, we summarize the recent functional magnetic resonance imaging (fMRI) studies conducted in our laboratory that test hypotheses about the nature of persistent activity during a variety of spatial cognition tasks. We find that the same areas in the PFC and PPC that show persistent activity during the maintenance of a working memory representation also show persistent activity during the maintenance of spatial attention and the maintenance of motor intention. Therefore, we conclude that persistent activity is not specific to working memory, but instead, carries information that can be used generally to support a variety of cognitions. Specifically, activity in topographically organized maps of prioritized space in PFC and PPC could be read out to guide attention allocation, spatial memory, and motor planning.

Perception and action selection dissociate human ventral and dorsal cortex.

We test theories about the functional organization of the human cortex by correlating brain activity with demands on perception versus action selection. Subjects covertly searched for a target among an array of 4, 8, or 12 items (perceptual manipulation) and then, depending on the color of the array, made a saccade toward, away from, or at a right angle from the target (action manipulation). First, choice response times increased linearly as the demands increased for each factor, and brain activity in several cortical areas increased with increasing choice response times. Second, we found a double dissociation in posterior cortex: Activity in ventral regions (occipito-temporal cortex) increased linearly with perceptual, but not action, selection demands; conversely, activity in dorsal regions (parietal cortex) increased linearly with action, but not perceptual, selection demands. This result provides the clearest support of the theory that posterior cortex is segregated into two distinct streams of visual processing for perception and action. Third, despite segregated anatomical projections from posterior ventral and dorsal streams to lateral pFC, we did not find evidence for a functional dissociation between perception and action selection in pFC. Increasing action, but not perceptual, selection demands evoked increased activation along both the dorsal and the ventral lateral pFC. Although most previous studies have focused on perceptual variables (e.g., space vs. object), these data suggest that understanding the computations underlying action selection will be key to understanding the functional organization of pFC.

Contralateral delay activity provides a neural measure of the number of representations in visual working memory.

Visual working memory (VWM) helps to temporarily represent information from the visual environment and is severely limited in capacity. Recent work has linked various forms of neural activity to the ongoing representations in VWM. One piece of evidence comes from human event-related potential studies, which find a sustained contralateral negativity during the retention period of VWM tasks. This contralateral delay activity (CDA) has previously been shown to increase in amplitude as the number of memory items increases, up to the individual's working memory capacity limit. However, significant alternative hypotheses remain regarding the true nature of this activity. Here we test whether the CDA is modulated by the perceptual requirements of the memory items as well as whether it is determined by the number of locations that are being attended within the display. Our results provide evidence against these two alternative accounts and instead strongly support the interpretation that this activity reflects the current number of objects that are being represented in VWM.

Cortical activity time locked to the shift and maintenance of spatial attention.

Attention increases the gain of visual neurons, which improves visual performance. How attention is controlled, however, remains unknown. Clear correlations between attention and saccade planning indicate that the control of attention is mediated through mechanisms housed in the oculomotor network. Here, we used event-related functional magnetic resonance imaging to compare overt and covert attention shifts. Subjects covertly or overtly shifted attention based on an endogenous cue and maintained attention throughout a long and variable delay. To insure continued attention, subjects counted when the attended target dimmed at near-threshold contrast levels. Overt and covert tasks used identical stimuli and required identical motor responses. Additionally, a staircase procedure that adjusted the target-dimming contrast separately for covert and overt trials equated the difficulty between conditions and across subjects. We found that the same regions along the precentral and intraparietal sulci were active during shifts of covert and overt attention. We also found sustained activation in the hemisphere contralateral to the attended visual field. We conclude that maps of prioritized locations are represented in areas classically associated with oculomotor control. The readout of these spatial maps by posterior visual areas directs spatial attention just as the readout by downstream saccade generators directs saccades.