Dynamic activation of frontal, parietal, and sensory regions underlying anticipatory visual spatial attention

Abstract

Although it is well established that multiple frontal, parietal, and occipital regions in humans are involved in anticipatory deployment of visual spatial attention, less is known about the electrophysiological signals in each region across multiple subsecond periods of attentional deployment. We used MEG measures of cortical stimulus-locked, signal-averaged (event-related field) activity during a task in which a symbolic cue directed covert attention to the relevant location on each trial. Direction-specific attention effects occurred in different cortical regions for each of multiple time periods during the delay between the cue and imperative stimulus. A sequence of activation from V1/V2 to extrastriate, parietal, and frontal regions occurred within 110 ms after cue, possibly related to extraction of cue meaning. Direction-specific activations ∼300 ms after cue in frontal eye field (FEF), lateral intraparietal area (LIP), and cuneus support early covert targeting of the cued location. This was followed by coactivation of a frontal-parietal system [superior frontal gyrus (SFG), middle frontal gyrus (MFG), LIP, anterior intraparietal sulcus (IPSa)] that may coordinate the transition from targeting the cued location to sustained deployment of attention to both space and feature in the last period. The last period involved direction-specific activity in parietal regions and both dorsal and ventral sensory regions [LIP, IPSa, ventral IPS, lateral occipital region, and fusiform gyrus], which was accompanied by activation that was not direction specific in right hemisphere frontal regions (FEF, SFG, MFG). Behavioral performance corresponded with the magnitude of attention-related activity in different brain regions at each time period during deployment. The results add to the emerging electrophysiological characterization of different cortical networks that operate during anticipatory deployment of visual spatial attention.

Figure 1.

Task design: covert anticipatory shifts of visual spatial attention. On each trial, a central arrow cue (50 ms duration) directed subjects to covertly deploy and hold their attention to the left (←‹) or right (›→) lower visual quadrant (continuously marked by circular gray patches). Following a 1 s delay, a second stimulus (S2, 80 ms duration) was delivered at either the cued or uncued location (50/50 probability of occurring at either location). Subjects performed a go/no-go discrimination of the S2 grating orientation only if it occurred at the cued location and ignored any stimuli presented at the uncued location. The S2 stimuli were categorized into four types: (cued vs uncued location) by (target orientation vs standard orientation). A 5 or 20° clockwise tilt of the grating orientation from vertical constituted a standard or target feature, respectively. The design produced an equal probability of receiving a relevant stimulus (i.e., S2 at the cued location) or an irrelevant distractor (i.e., S2 at the uncued location) and required performance of a feature discrimination at the relevant spatial location. The size of the arrow cue is larger, and the contrast level of gratings is exaggerated for easier visualization.

Figure 2.

Anatomical ROIs. The locations and extents of the 11 ROIs (yellow patches) are illustrated from different views of the inflated cortex of the right hemisphere (although ROIs were used in both hemispheres, only the right is illustrated here for simplification of viewing). Light and dark gray correspond with gyri and sulci, respectively. Top left, Anterior view of right hemisphere. Top right, Posterior view of right hemisphere. Bottom left, Lateral view of right hemisphere. Bottom right, Medial view of right hemisphere. Fusiform, Fusiform gyrus; V1/V2, early-tier visual sensory cortices in the vicinity of V1/V2; SFG, superior frontal gyrus; MFG, middle frontal gyrus; FEF, frontal eye field; IPL, inferior parietal lobe; IPSa, anterior intraparietal sulcus anterior; LIP, lateral intraparietal area; IPSv, ventral intraparietal sulcus ventral; LO, lateral occipital region.

Figure 3.

Method for deriving direction-specific anticipatory visual attention effects. Direction-specific attention effects on brain activity are defined in the ANOVA model as interaction effects between factors cue direction (left, right) and ROI-hemisphere (left, right). An example of such an interaction is graphed at the top. ROI activity is measured in the left and right hemisphere under two conditions: when spatial attention is cued toward or away from the visual field contralateral to the ROI hemisphere, corresponding to conditions in which the spatial location contralateral to the cortical region is attended or unattended, respectively. For example in the right hemisphere ROI, cue left–cue right conditions correspond to attended–unattended conditions. Comparison between the same conditions (cue left–cue right) for the left hemisphere should reveal the effect with opposite sign because this comparison corresponds to unattended–attended conditions. This interaction effect appears graphically as a nonzero slope between the values for the left and right hemispheres. An example is illustrated in the figure for IPSa. The IPSa MEG activity waveforms for each condition (cue left and cue right) are plotted in the middle. The a priori time window for defining the amplitudes entered into the ANOVA (400–500 ms in this example) is shown by the vertical box. (Note that to capture the activity predicted by the literature, each a priori time window is divided into two equal subwindows due to variance in the latencies from the literature. The data shown in the plot in the top panel are for the 400–450 ms subwindow.) The mean amplitude during the subwindow is determined for each attention condition, and the resultant value for subtracting cue left and cue right mean amplitudes for a hemisphere is plotted in the top panel, reflecting the attention effect in that hemisphere.

Figure 4.

Early onsets of activity across cortical regions. The waveforms illustrate the initial onsets of activity to the cue stimulus from representative ROIs in occipital (V1/V2; cuneus), parietal (IPL), and frontal lobes (FEF, MFG). The waveforms show differences in onset timing consistent with conduction time between regions and indicate that bottom-up processing of cue information has occurred throughout these regions by ∼110 ms after cue.

Figure 5.

Earliest (150–175 ms) direction-specific effect. The first statistically significant direction-specific attentional modulation of cortex was found in the occipital cuneus region during the 150–175 ms period following the cue. The cue by hemisphere interaction effect in the cuneus is illustrated in the right panel: the difference in MEG magnitude between the two attention conditions (cue left − cue right) is shown for the LH and RH cuneus regions.

Figure 6.

Early period (250–350 ms): direction-specific attention system. The early period, 250–350 ms after cue, significant direction-specific attention effects occurred in a parietal and occipital system involving LIP and cuneus regions. In addition, there was a trend effect in the LO region (p = 0.052) shown in the plots of attention effects. The cue by hemisphere attention effects are illustrated in the right panels for the subwindows of the early period (250–300 and 300–350 ms).

Figure 7.

Middle period (400–500 ms): direction-specific attention system. Direction-specific processing in the middle period (400–500 ms after cue) during anticipatory attentional deployment occurred in a different system involving prefrontal and parietal control regions—SFG, MFG, LIP and IPSa—and did not involve sensory regions.

Figure 8.

Late period (800–1000 ms): direction-specific attention system and frontal attention system. The final period during anticipatory attentional deployment leading up to the onset of the imperative stimulus (800–1000 ms after cue) involved two cortical systems. One system was related to direction-specific processes, and the other system was comprised of right hemisphere frontal regions (indicated by white patches and labels). This frontal system had late sustained activity that was significantly above precue baseline levels but was not direction specific, consistent with a top-down control anticipatory role. The direction-specific attention system includes a different configuration of parietal regions (LIP, IPSa, IPSv) relative to preceding periods, and, in contrast to the early period, having modulation only in dorsal occipital regions, this final system involves both dorsal (LO) and ventral (fusiform) occipital regions, consistent with attention-related modulation based on both location and feature aspects of the anticipated target. In the frontal system, the right hemisphere frontal regions, the FEF, SFG and MFG, have significantly increased levels of activity during the final period of anticipatory attention.