Choosing where to attend and the medial frontal cortex: an FMRI study

Abstract

To investigate how we orient our spatial attention, previous studies have recorded neural activity while participants are instructed where to attend. Here we contrast this classical instructed attention condition with a novel condition in which the focus of voluntary attention is not specified by the experimenter but rather is freely chosen by the participant. Central cues prompted fixating participants either to choose which of two peripheral spatial locations to covertly attend or formed an instruction. Either type of cueing initiated selective attention demonstrated behaviorally by enhanced performance at a visual detection task in comparison to a separate divided attention condition. We used functional magnetic resonance imaging to measure which areas were more active during choice than instruction. Choosing where to attend activated a large cluster of medial frontal cortical regions similar to those that have been previously implicated in the free selection of overt action. We then addressed a potential confound in contrasting choice with instruction: participants may remember their behavior more when choosing. In a separate block, and interleaved with choice trials, "memory" trials were introduced in which participants were instructed to remember where they had attended on the previous trial. The presupplementary eye fields and lateral frontal eye fields were specialized for choice-guided attentional orienting over and above any memory confound. This evidence suggests a common mechanism may underlie free selection, whether for covert attention or overt saccades.

FIG. 1.

Task schematic. On instructed trials, the “l” or “r” of the central precue was red, and participants were to covertly attend to the left or right stream of letters. But on choice trials, if the horizontal line was red (shown here in gray) then the participants themselves freely selected which side to attend. Participants responded when they detected the target letter “a”. This figure shows the spatial block; in the memory block the letters were “s” or “d” (instructing the participant to attend to the “same” or “different” side as the previous trial) rather than “l” or “r”.

FIG. 2.

Behavioral data. Participants covertly oriented their selective attention on both choice and instructed trials of the spatial block (A and B) and the memory block (C and D), shown as improved accuracy compared with divided attention trials (A and C) without any reaction time trade-off (B and D). Bars show SE.

FIG. 3.

A single contiguous cluster of medial frontal cortical regions were more active during choosing where to attend than being instructed [choice > instructed, across both spatial and memory blocks, time-locked to cue onset, overlaid on the average structural magnetic resonance image (MRI) from all participants, corrected for multiple comparisons (thresholded at z = 2.3, cluster P = 0.01)]. Left: cross-hairs on MNI (x,y,z) coordinates 14, 10, 62 [right presupplementary eye field (pre-SEF)]. Right: cross-hairs on 4, 18, 36 [right (ACC)].

FIG. 4.

Location of each ROI. ROIs in the left hemisphere are numbered in the order presented in Table 2, i.e., 1, left lateral frontal eye field; 2, left medial frontal eye field; 3, left dorsal intraparietal sulcus; 4, left ventral intraparietal sulcus; 5, left supplementary eye field; 6, left presupplementary eye field; 7, left anterior cingulate cortex; 8, left presupplementary motor area; 9, left angular gyrus. To show all ROIs, cross-sections are taken with the cross-hairs within the left presupplementary motor area (left) and the left anterior cingulate cortex (right). Note that all ROIs are of equal volume but the medial ROIs are rectangular cuboids to prevent overlap.

FIG. 5.

Histograms showing mean % blood-oxygen-level-dependent (BOLD) change from baseline signal within each region of interest (ROI). ROIs that showed a main effect of hemisphere are shown for each hemisphere. A: medial areas. B: parietal areas. C: frontal areas (spatial, spatial block; memory, memory block, choice, choice trials; instr, instructed trials. Only left pre-SEF and lateral FEF showed more activity on choice than instructed trials in both the spatial and memory blocks.