Cortical and Subcortical Coordination of Visual Spatial Attention Revealed by Simultaneous EEG-fMRI Recording

Abstract

Visual spatial attention has been studied in humans with both electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) individually. However, due to the intrinsic limitations of each of these methods used alone, our understanding of the systems-level mechanisms underlying attentional control remains limited. Here, we examined trial-to-trial covariations of concurrently recorded EEG and fMRI in a cued visual spatial attention task in humans, which allowed delineation of both the generators and modulators of the cue-triggered event-related oscillatory brain activity underlying attentional control function. The fMRI activity in visual cortical regions contralateral to the cued direction of attention covaried positively with occipital gamma-band EEG, consistent with activation of cortical regions representing attended locations in space. In contrast, fMRI activity in ipsilateral visual cortical regions covaried inversely with occipital alpha-band oscillations, consistent with attention-related suppression of the irrelevant hemispace. Moreover, the pulvinar nucleus of the thalamus covaried with both of these spatially specific, attention-related, oscillatory EEG modulations. Because the pulvinar's neuroanatomical geometry makes it unlikely to be a direct generator of the scalp-recorded EEG, these covariational patterns appear to reflect the pulvinar's role as a regulatory control structure, sending spatially specific signals to modulate visual cortex excitability proactively. Together, these combined EEG/fMRI results illuminate the dynamically interacting cortical and subcortical processes underlying spatial attention, providing important insight not realizable using either method alone.SIGNIFICANCE STATEMENT Noninvasive recordings of changes in the brain's blood flow using functional magnetic resonance imaging and electrical activity using electroencephalography in humans have individually shown that shifting attention to a location in space produces spatially specific changes in visual cortex activity in anticipation of a stimulus. The mechanisms controlling these attention-related modulations of sensory cortex, however, are poorly understood. Here, we recorded these two complementary measures of brain activity simultaneously and examined their trial-to-trial covariations to gain insight into these attentional control mechanisms. This multi-methodological approach revealed the attention-related coordination of visual cortex modulation by the subcortical pulvinar nucleus of the thalamus while also disentangling the mechanisms underlying the attentional enhancement of relevant stimulus input and those underlying the concurrent suppression of irrelevant input.

Keywords: EEG; attentional control; fMRI; pulvinar; visual cortex.

Figure 1.

Schematic diagram of a target present trial (see text for details).

Figure 2.

Average BOLD signal (p < 0.01, FDR corrected, k = 25). Attentional control regions identified from the attend cue versus interpret cue BOLD contrast (top row) and spatially specific occipital activations identified from contrasting activity for leftward-directing versus rightward-directing cues.

Figure 3.

Average event-related responses and scalp topographies of contralateral-minus-ipsilateral differences for alpha-band (top) and gamma-band (bottom) EEG. Light gray boxes denote time windows with significant (p < 0.05) differences between ipsilateral and contralateral electrodes that were used for covariational analyses.

Figure 4.

Covariations in the pulvinar. Early gamma for attend cues (left and right) positively covaried with BOLD signal in the pulvinar and early visual cortex (p < 0.001 uncorrected, k > 25; top). This contrast was then used to create functional ROIs in the left and right pulvinar (bottom). Both ipsilateral alpha and late contralateral gamma showed spatially specific positive covariations in the pulvinar ROIs (significant cue direction × hemisphere interaction). Early gamma covariations are shown only for comparative purposes because these regions were originally defined by having significant early gamma covariation activity. *p < 0.05; **p < 0.01.

Figure 5.

Covariation between BOLD and ipsilateral alpha (top) and contralateral late gamma (bottom). Alpha was negatively correlated with occipital and parietal BOLD activity in the hemisphere ipsilateral to the cued location, whereas late gamma was positively correlated with occipital BOLD signal contralateral to the cued location. p < 0.001 uncorrected, k = 25.

Figure 6.

Covariations within functional ROIs based on the alpha covariation (cyan and blue bars) and occipital (red and orange bars) and parietal (purple and magenta bars) BOLD responses. Spatially specific alpha and late-gamma covariations (significant hemisphere × cue direction interaction) occurred in distinct regions of visual cortex. Alpha covariations within the alpha-defined ROIs are shown for comparative purposes only because these regions were defined by having significant alpha covariation activity. Some evidence of spatially specific covariations was also seen in the parietal regions for alpha and late gamma, but these interactions did not reach significance. *p < 0.05; **p < 0.01; ***p < 0.001.