Neural correlates of perceptual choice and decision making during fear-disgust discrimination

Abstract

In the present study, we tested the hypothesis that brain activation would reflect perceptual choices. To probe this question, we used functional magnetic resonance imaging (fMRI) during a challenging fear-disgust, two-choice discrimination task. We investigated how moment-to-moment fluctuations in fMRI signals were correlated with perceptual choice by computing a choice probability index that quantified how well behavioral choice could be predicted by single-trial fMRI amplitude. Our analyses revealed that reporting a neutral face as "fearful" was associated with activation in a broad network of brain regions that process emotionally arousing stimuli, whereas reporting a neutral face as "disgusted" was associated with activation in a focused set of sites that included the putamen and anterior insula. Responses predictive of perceptual reports were not only observed at the group level but also at the single-subject level. Thus, voxel-by-voxel fluctuations in fMRI amplitude for an individual participant could be used to reliably predict the perceptual choice of individual trials for that subject. In addition to the investigation of choice, we also isolated the neural correlates of decision making per se by using reaction time as an index of decision processes. Overall, our findings revealed that brain responses dynamically shifted according to perceptual choices. In addition, the neural correlates of decision making involved at least the anterior cingulate cortex, middle frontal gyrus, and inferior frontal gyrus/insula, consistent with recent proposals that decisions may emerge from distributed processes.

Figure 1.

A, Example of the graded emotional facial expressions used in the task ranging from 100% disgusted to 100% fearful. B, Representative behavioral response pattern of a subject showing the rate of fearful responses (y-axis) as a function of graded stimulus level (x-axis). The overall pattern exhibits a sigmoidal shape that was significantly fit by a Weibull function (p < 0.05); the filled black dot depicts the 50% point of the fitted curve. C, Group activation map for the contrast of 100% fearful/disgusted stimuli versus baseline. The task robustly activated regions along occipitotemporal cortex, including bilateral fusiform gyrus, as well as the amygdala, bilaterally. The bar plots show activation strength in the amygdala for different levels of graded stimuli (the white arrows indicate the corresponding left/right amygdala of origin). Note that no significant differences were observed for fearful and disgusted stimuli at corresponding stimulus levels (e.g., 100% disgusted and fearful). The level of the slice is indicated according to the MNI template. L, Left; R, right.

Figure 2.

Group choice probability map. A, Group choice map based on trials with neutral faces. Voxels whose fMRI signals predicted fearful responses are depicted in red/yellow, and voxels whose fMRI signals predicted disgusted responses are depicted in blue. B, Combined group map depicting choice-related activation (red), stimulus-related activation (blue), and their intersection (green). Interestingly, there was little overlap in the activations, but they neighbored each other in the left anterior insula and the right IFG/IFS. The levels of the slices are indicated according to the MNI template. L, Left; R, right; SPG, superior parietal gyrus.

Figure 3.

Average ROC curves for representative ROIs predictive of fearful and disgusted responses. Average ROC curves for the right anterior IFG and right putamen/insula ROIs. The curves were constructed by determining the most predictive voxel within the ROI for each subject; the ROC curves of these voxels were then averaged across subjects to yield the mean curve. The error bars and gray-level bands depict the region of the mean ± SD.

Figure 4.

Distribution of choice probability values. Median choice probability values (1 value for each subject) for the regions listed in Table 1. Choice probability values (x-axis) >0.5 indicate regions predictive of fearful reports (red), and choice probability values smaller than 0.5 indicate regions predictive of disgusted reports (blue). The y-axis shows the subject count. All distributions are clearly skewed to the right (columns 1, 2) or left (column 3), illustrating the consistency of the selectivity for both fearful and disgusted reports, respectively.

Figure 5.

Neural correlates of decision making. The correlates of decision making were isolated by using RT as an index of decision processes. Activated voxels met our criteria for decision-related activation (see Results). In the ACC and the anterior insula, the average fMRI response as a function of condition exhibited an inverted-U pattern that closely matched the pattern of average RTs (see insets). The levels of the slices are indicated according to the MNI template. L, Left; R, right.