An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention

Abstract

Attention can be voluntarily directed to a location or automatically summoned to a location by a salient stimulus. We compared the effects of voluntary and stimulus-driven shifts of spatial attention on the blood oxygenation level-dependent signal in humans, using a method that separated preparatory activity related to the initial shift of attention from the subsequent activity caused by target presentation. Voluntary shifts produced greater preparatory activity than stimulus-driven shifts in the frontal eye field (FEF) and intraparietal sulcus, core regions of the dorsal frontoparietal attention network, demonstrating their special role in the voluntary control of attention. Stimulus-driven attentional shifts to salient color singletons recruited occipitotemporal regions, sensitive to color information and part of the dorsal network, including the FEF, suggesting a partly overlapping circuit for endogenous and exogenous orienting. The right temporoparietal junction (TPJ), a core region of the ventral frontoparietal attention network, was strongly modulated by stimulus-driven attentional shifts to behaviorally relevant stimuli, such as targets at unattended locations. However, the TPJ did not respond to salient, task-irrelevant color singletons, indicating that behavioral relevance is critical for TPJ modulation during stimulus-driven orienting. Finally, both ventral and dorsal regions were modulated during reorienting but significantly only by reorienting after voluntary shifts, suggesting the importance of a mismatch between expectation and sensory input.

Figure 1.

a, Examples of the three cueing conditions in the experiment. Each trial began with a central fixation point surrounded by a diamond. The cue display then appeared for 100 ms. After an ISI, the target letter (T or L) appeared in either the left or right location for 150 ms. During the behavioral (Beh.) experiment, ISIs were either 50 or 600 ms, corresponding to cue-target SOAs of 150 and 700 ms, where as, in the fMRI experiment, the ISI and SOA were 2060 and 2160 ms, respectively. Participants made a two-alternative forced-choice decision regarding the identity of the letter (T vs L). b, Group-averaged RT data from the behavioral session. c, Group-averaged RT data from the fMRI session.

Figure 2.

Cue period. Voxels with a significant interaction of cue type (exogenous, endogenous, and neutral) by time in a group ANOVA, corrected for multiple comparisons, are shown. Because no voxels showed a significant interaction in right ventral frontoparietal regions (IFG and TPJ), ROIs for these regions were determined from the voxelwise map of the interaction of validity by time during the target period in the endogenous condition (ROIs defined by black outlines). Group-averaged time courses are shown for four dorsal-frontal parietal regions that showed significant cue type by time interactions in the voxel-level map and for the two ventral ROIs defined from the target period.

Figure 3.

Cue period. Voxels in the lateral occipital cortex (LO) and the anterior fusiform (Fus) with a significant interaction of cue type (exogenous and endogenous) by time in a group ANOVA, corrected for multiple comparisons, are shown. Group-averaged time courses are also shown.

Figure 4.

Target period. Voxels with a significant interaction of cue type (exogenous and endogenous) by validity by time in a group ANOVA, corrected for multiple comparisons (FEF, SMG, and insula), are shown. For comparison, the regions in the IFG and SMG defined by the interaction of validity by time in the endogenous condition are also shown (black outline). Group-averaged time courses are also shown for the cue type by validity by time interaction ROIs, with the exception of the right IFG shown from the validity by time in the endogenous condition only.