Dissociable Decoding of Spatial Attention and Working Memory from EEG Oscillations and Sustained Potentials

Abstract

In human scalp EEG recordings, both sustained potentials and alpha-band oscillations are present during the delay period of working memory tasks and may therefore reflect the representation of information in working memory. However, these signals may instead reflect support mechanisms rather than the actual contents of memory. In particular, alpha-band oscillations have been tightly tied to spatial attention and may not reflect location-independent memory representations per se. To determine how sustained and oscillating EEG signals are related to attention and working memory, we attempted to decode which of 16 orientations was being held in working memory by human observers (both women and men). We found that sustained EEG activity could be used to decode the remembered orientation of a stimulus, even when the orientation of the stimulus varied independently of its location. Alpha-band oscillations also carried clear information about the location of the stimulus, but they provided little or no information about orientation independently of location. Thus, sustained potentials contain information about the object properties being maintained in working memory, consistent with previous evidence of a tight link between these potentials and working memory capacity. In contrast, alpha-band oscillations primarily carry location information, consistent with their link to spatial attention. Working memory plays a key role in cognition, and working memory is impaired in several neurological and psychiatric disorders. Previous research has suggested that human scalp EEG recordings contain signals that reflect the neural representation of information in working memory. However, to conclude that a neural signal actually represents the object being remembered, it is necessary to show that the signal contains fine-grained information about that object. Here, we show that sustained voltages in human EEG recordings contain fine-grained information about the orientation of an object being held in memory, consistent with a memory storage signal.

Hemispheric asymmetries in posterior alpha power reflect the selection and inhibition of spatial context information in working memory

“…However, hemispheric asymmetries in alpha power were not modulated by the number of cued or non-cued items and were thus unrelated to the selection/inhibition of non-spatial information content (here: representation of different color values). This finding is in line with the notion that posterior alpha power is related to the spatial orienting of attention (Bae & Luck, 2018;Hakim, Adam, Gunseli, Awh, & Vogel, 2019). Importantly, we showed that withdrawing the focus of attention from the position of lateral working memory content involved an inhibitory attentional control process (see figure 3A and 3B).…”

“…Here, we assessed retinotopic modulations of posterior alpha power by focusing on posterior hemispheric asymmetries (see figure 3). As hypothesized, alpha power lateralization was insensitive to the number of cued or non-cued working memory items, in line with its role in the spatial orienting of attention (Bae & Luck, 2018;Hakim et al, 2019). While this insensitivity of posterior alpha power asymmetries to the number of cued vs. non-cued items was already indicated by an earlier investigation (Poch, Carretie, & Campo, 2017), we further corroborate the notion that the spatial orienting of the focus of attention in working memory is based on inhibition: As indicated in figure 3, hemispheric asymmetries in alpha power differed between conditions with lateral targets and lateral distractors.…”

“…We now extended this experimental design by furthermore including varying set-sizes of the memory arrays and a control condition with a neutral retro-cue for a clear interpretation of hemispheric asymmetries as correlates of distractor inhibition vs. target enhancement. As prior investigations linked posterior alpha asymmetries to the spatial orienting of attention (Bae & Luck, 2018;Hakim, Adam, Gunseli, Awh, & Vogel, 2019), they should be independent of the number of cued vs. non-cued working memory representations. We further expected to replicate our prior finding of an increase in posterior alpha power contralateral to non-cued working memory contents and a respective decrease in oscillatory power contralateral to the position of cued items.…”

Inhibition in selective attention

“…This apparent discrepancy can be explained by assuming a flexible locus of distractor suppression, which either in case of only spatial regularities operates at the level of spatial priority maps, or in case of additional feature expectations operates at so‐called conspicuity maps coding specific feature dimensions . Given the tight link between alpha‐band activity and spatial attention, suppression operating at spatial priority maps likely relies on modulations of alpha oscillations. More work, however, is necessary to determine the functional significance of alpha‐band oscillatory activity, especially since recent work indicates that alpha oscillations may not signal top‐down inhibition of cortical activity per se, but stabilization of the current configuration of neuronal activity, possibly through enhancing signal‐to‐noise .…”

Enhancing multivariate pattern analysis for magnetoencephalography through relevant sensor selection

“…Together with representational similarity analysis, 2 MVPA has demonstrated promising capabilities in revealing subtle neural signature of cognitive processes in magnetoencephalography (MEG), electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) data. [3][4][5][6][7][8][9][10][11][12][13][14][15] In many neuroimaging studies, 4,[16][17][18] the pattern vector dimension (number of M/EEG channels or fMRI voxels) highly exceeds the number of data samples (experimental trials), thus incurring the "curse of dimensionality," 19,20 which consequently deteriorates the classifier performance.…”