High-resolution BOLD fMRI measurements of local orientation-dependent contextual modulation show a mismatch between predicted V1 output and local BOLD response

Abstract

The blood oxygenation level-dependent (BOLD) functional MRI response to suppressive neural activity has not been tested on a fine spatial scale. Using Gabor patches placed in the near periphery, we precisely localized individual regions of interest in primary visual cortex and measured the response at a range of contrasts in two different contexts: with parallel and with orthogonal flanking Gabor patches. Psychophysical measurements confirmed strong suppression of the target Gabor response when flanked by parallel Gabors. However, the BOLD response to the target with parallel flankers decreased as the target contrast increased, which contradicts psychophysical estimates of local neural activity.

Figure 1

Stimuli used to study contextual modulation in V1. (A) Targets alone (top) and targets with flankers (bottom) block localizer scans. Stimuli were presented in the same 2IFC paradigm, 6 trials per 12 second block. During “blank” blocks subjects performed a 2IFC contrast detection task with a 0% target pedestal contrast. Ten and one half cycles were completed per scan. (B) Stimuli for event related scans: targets with parallel flankers (target contrast was 8%, 16%, or 32%), targets with orthogonal flankers (again, target contrast was 8%, 16%, or 32%), targets alone (32% contrast on all trials), and flankers alone (50% contrast). Stimuli were presented in a 2-interval forced choice (2IFC) paradigm (stimulus duration: 250 ms, inter-stimulus interval (ISI): 500 ms) Inter-trial interval was 3, 4.5 or 6 seconds (randomly selected for each trial).

Figure 2

Psychophysical quantification of suppression of target Gabor responses by flanking Gabor patches. The top row has threshold versus contrast plots (red: parallel flankers, blue: orthogonal flankers, black: targets alone) while the bottom row shows inferred contrast response functions (calculated after fitting threshold versus contrast data with a variant of the Naka-Rushton formula, equations 1 and 2). Each column contains the result from a single subject. High contrast discrimination thresholds for the targets with parallel and orthogonal flankers translated to a low inferred neural response in the contrast response function (CRF) compared to the targets-alone configuration for all three subjects. Psychophysical measurements predict parallel flankers will suppress neural response to target Gabors 20 – 50% when the targets are at 16% contrast.

Figure 3

ROI localization. (A) Functional data from target block localizers (averaged data from three days, a total of 9 target-alone localizer scans), for one subject (S3), overlaid on mean functional image (color map: blue indicates in-phase with stimulus presentation, red indicates out of phase with stimulus presentation). Target ROI is indicated by white outline, superset ROI (identified by a different set of functional data) is indicated by dark green outline. Two of four sub-ROIs are visible in this particular slice; the other two sub-ROIs are located in different slices. (B) Target ROIs from three different days for the same subject, translated to the reference anatomy (1 mm isotropic resolution) and shown on a single coronal slice (Blue: Day 1, Green: Day 2, Red: Day 3). (C) Three-dimensional plots of all target ROI locations for all subjects for three days. For each subject, each sub-ROI is represented by a cube centered at the calculated center of mass (COM). The volume of the cube indicates the volume of the sub-ROI. Indicated above each plot is the average pairwise 3D Euclidian distance between sub-ROI COMs from the three different days (n=12 comparisons, 3 for each of 4 locations, for each subject).

Figure 4

Estimated BOLD fMRI responses in target ROI. (A-C) BOLD fMRI responses from one subject (S1), averaged over three scanning sessions. Target-alone condition is shown in black. (A) In the target ROI, the flanker-alone conditions (green lines) dominate even though no target Gabor patch is present. (B) Peak BOLD response increases with an increase in target contrast with orthogonal flankers. (C) Peak BOLD response decreases with an increase in target contrast with parallel flankers. (D-E) Response amplitude is estimated as the amplitude of a difference-of-gamma functions HRF model fit to the estimated HRFs, and error bars represent SEM. Significant interaction was found between the parallel and orthogonal conditions (p < 0.05, 2-way ANOVA). (D) Summary of peak BOLD amplitude over all subjects, target ROIs (individual day data, n=9). (E) Summary of peak BOLD amplitude over all subjects, superset ROIs (individual day data, n=9). Similar patterns of results were obtained for both the target (D) and superset (E) ROIs.

Figure 5

Discrimination thresholds for parallel flankers with 50% pedestal contrast, under three different target contrast conditions (8%, 16%, 32% pedestal contrast); error bars are SEM (n = 3 threshold estimates per subject). Thresholds decreased with increasing target contrast for both subjects, which would not be the case if flanker response was suppressed by targets of higher contrast.

Figure 6

BOLD response to target-alone Gabor patches at 8%, 16%, and 32% pedestal contrast. Contrast response functions for individual subjects were normalized by the response to the 32% contrast stimulus and averaged (n = 3, error bars indicate SEM).

Figure 7

Annulus experiment results: BOLD response to the center annulus increases with increasing contrast, in spite of the presence of the parallel surround. Error bars represent SEM (n=6 hemispheres). The response to a 40% contrast center annulus is suppressed 21% by the presence of a parallel surround.