Spatial selectivity in the temporoparietal junction, inferior frontal sulcus, and inferior parietal lobule

Abstract

Spatial selectivity, as measured by functional magnetic resonance imaging (fMRI) activity patterns that vary consistently with the location of visual stimuli, has been documented in many human brain regions, notably the occipital visual cortex and the frontal and parietal regions that are active during endogenous, goal-directed attention. We hypothesized that spatial selectivity also exists in regions that are active during exogenous, stimulus-driven attention. To test this hypothesis, we acquired fMRI data while subjects maintained passive fixation. At jittered time intervals, a briefly presented wedge-shaped array of rapidly expanding circles appeared at one of three contralateral or one of three ipsilateral locations. Positive fMRI activations were identified in multiple brain regions commonly associated with exogenous attention, including the temporoparietal junction, the inferior parietal lobule, and the inferior frontal sulcus. These activations were not organized as a map across the cortical surface. However, multivoxel pattern analysis of the fMRI activity correctly classified every pair of stimulus locations, demonstrating that patterns of fMRI activity were correlated with spatial location. These observations held for both contralateral and ipsilateral stimulus pairs as well as for stimuli of different textures (radial checkerboard) and shapes (squares and rings). Permutation testing verified that the obtained accuracies were not due to systematic biases and demonstrated that the findings were statistically significant.

Trial registration: ClinicalTrials.gov NCT01087281.

Figures

Figure 1

Stimuli. Left: Schematics showing the stimulus locations. The lines pictured in the schematics did not appear in the stimuli. Right: Example stimulus presentations. Numbers indicate each frame's duration and root mean square contrast.

Figure 2

(A) ROIs derived from Experiment 4 data and used for MVPA analysis of data from Experiments 1 through 3. (B) ROIs derived from Experiment 1 data and used for MVPA analysis of data from Experiment 4. (C) VC ROI derived from anatomical landmarks and used for MVPA analysis of data from Experiments 1 through 4.

Figure 3

MVPA prediction accuracies, Experiment 1. Each matrix provides accuracy predictions derived from one ROI. The color of each element in a matrix represents the mean percentage correct, averaged across subjects, of a particular condition pair's MVPA predictions. For example, the element in the top right corner of each matrix represents the percentage of correct classifications of wedges presented on the right at horizontal versus on the lower right. Chance performance would be 50% (green). Predictions for all condition pairs were substantially more accurate than chance.

Figure 4

MVPA prediction accuracies, Experiment 2. Each matrix provides accuracy predictions derived from one ROI. The color of each element in a matrix represents the mean percentage correct, averaged across subjects, of a particular condition pair's MVPA predictions. For example, the element in the top right corner of each matrix represents the percentage of correct classifications of wedges presented on the right at horizontal versus on the lower right. Chance performance would be 50% (green). Predictions for all condition pairs were substantially more accurate than chance.

Figure 5

MVPA prediction accuracies, Experiment 3. Each matrix provides accuracy predictions derived from one ROI. The color of each element in a matrix represents the mean percentage correct, averaged across subjects, of a particular condition pair's MVPA predictions. For example, the element in the top right corner of each matrix represents the percentage of correct classifications of squares presented on the right at horizontal versus on the lower right. Chance performance would be 50% (green). Predictions for all condition pairs were substantially more accurate than chance.

Figure 6

MVPA prediction accuracies, Experiment 4. Each matrix provides accuracy predictions derived from one ROI. The color of each element in a matrix represents the mean percentage correct, averaged across subjects, of a particular condition pair's MVPA predictions. For example, the element in the top right corner of each matrix represents the percentage of correct classifications of rings presented closest to versus farthest from the fixation point. Chance performance would be 50% (green). Predictions for all condition pairs were substantially more accurate than chance.

Figure 7

Mean MVPA prediction accuracies, all experiments. (A) Accuracies of predictions derived from the data in Experiments 1 through 3 within the ROIs derived from the Experiment 4 data. The height of each bar represents the mean percentage correct, averaged across subjects and condition pairs, of the MVPA predictions; error bars represent ±1 SD across condition pairs. Chance performance would be 50%. In all cases prediction accuracy was significantly greater than chance. Asterisks indicate p < 10−18; p values were obtained by performing a one-sample t test on the results of the within-subject, within-condition-pair permutation tests. (B) Accuracies of predictions derived from the data in Experiment 4 within the ROIs derived from the Experiment 1 data.

Figure 8

MVPA prediction accuracies in the downsampled VC ROI. A subset of data points was randomly sampled from the VC ROI such that the downsampled VC ROI and the other ROIs were the same size. In this figure, each matrix provides accuracy predictions derived from the downsampled VC ROI in one experiment. The color of each element in a matrix represents the mean percentage correct, averaged across subjects, of a particular condition pair's MVPA predictions. For example, the element in the top right corner of the Experiment 1 matrix represents the percentage of correct classifications of wedges presented on the right at horizontal versus on the lower right. Chance performance would be 50% (green). Predictions for all condition pairs were substantially more accurate than chance.

Figure 9

Mean MVPA prediction accuracy differences for nonadjacent versus adjacent stimulus pairs, all experiments. Stars indicate a difference significantly (p < 0.05) greater than zero as measured by a one-tailed t test across subjects and stimulus pairs. In the VC, but not in the remaining ROIs, nonadjacent stimulus pairs predicted better than adjacent stimulus pairs in Experiments 1, 2, and 4. (Note that in Experiment 3, none of the stimuli were literally adjacent, so a reduced prediction advantage in the VC for Experiment 3 relative to Experiment 1 is expected.)

Figure 10

Voxelwise preferred angle and eccentricity estimates in an example subject. Preferred angles were calculated using the polar mean on the GLM activations from Experiment 1; preferred eccentricities were calculated using the center of mass on the GLM activations from Experiment 4. Despite the coarse spatial resolution used in our whole-brain design, topographic organization was evident in the early VC. We did not observe topographic organization in the other ROIs.

Figure 11

Activation levels in response to ipsilateral horizontal stimuli in Experiment 3. The height of each bar indicates the mean activity level of fMRI responses to contralateral and ipsilateral squares at the horizontal meridian. The means were calculated within ROI across subjects on positive fMRI activations only. That is, voxels with a positive response to contralateral squares were averaged for the contralateral mean, and voxels with a positive response to ipsilateral squares were averaged for the ipsilateral mean. Stars indicate a contralateral versus ipsilateral difference significantly (p < 0.05) greater than zero as measured by a one-tailed t test across voxels in all subjects. The activations used in the calculations were the outputs of a GLM in which regressors represented model responses to the entire series of stimulus presentations at each location. A contralateral preference was evident in the VC and FG only. In the remaining ROIs, positive activations to the ipsilateral horizontal meridian were roughly equal in magnitude to positive activations to the contralateral horizontal meridian.