Prefrontal contributions to metacognition in perceptual decision making

Abstract

Neuroscience has made considerable progress in understanding the neural substrates supporting cognitive performance in a number of domains, including memory, perception, and decision making. In contrast, how the human brain generates metacognitive awareness of task performance remains unclear. Here, we address this question by asking participants to perform perceptual decisions while providing concurrent metacognitive reports during fMRI scanning. We show that activity in right rostrolateral prefrontal cortex (rlPFC) satisfies three constraints for a role in metacognitive aspects of decision-making. Right rlPFC showed greater activity during self-report compared to a matched control condition, activity in this region correlated with reported confidence, and the strength of the relationship between activity and confidence predicted metacognitive ability across individuals. In addition, functional connectivity between right rlPFC and both contralateral PFC and visual cortex increased during metacognitive reports. We discuss these findings in a theoretical framework where rlPFC re-represents object-level decision uncertainty to facilitate metacognitive report.

Figure 1.

Perceptual decision task. On each trial, participants were asked to categorize a noisy image as either a face or a house by pressing one of two buttons held in their right hand. In the Report condition, post-decision confidence was indicated using a sliding scale. In the Follow condition, participants were instructed to slide the cursor into the zone indicated by the two vertical lines. After 3.5 s, the cursor changed color to indicate the participant's selected rating.

Figure 2.

Behavioral results. A, Performance split according to reported confidence (calculated from subject-specific tertiles). B, Perceptual task performance (d′) as a function of metacognition task condition. Error bars in A and B reflect the SEM. C, Plot of the relationship between metacognitive accuracy (A_roc) and percentage correct on Report trials, with participants ordered such that A_roc increases from left to right.

Figure 3.

fMRI results. Activation in the contrasts Report > Follow (hot colors) and Follow > Report (cool colors) displayed at p < 0.001, uncorrected. Color bar reflects t-statistic. Significant clusters corrected for multiple comparisons at p < 0.05 are listed in Table 1.

Figure 4.

fMRI results. A, Activation correlating negatively with confidence on Report trials, inclusively masked by Report > Follow. All clusters are significant at p < 0.05, corrected for multiple comparisons; images are displayed at p < 0.001, uncorrected. L, Left; R, right. B, Parameter estimates for the correlation between confidence and activity in each ROI, split according to condition. Gray bars (Report condition) are displayed only to indicate effects of equal magnitude on face and house trials, significance having been previously established in the SPM from part A. No correlation with confidence was seen in these ROIs on Follow trials (white bars; one-sample t test against zero, p > 0.1). Error bars reflect the SEM. C, Time courses from each ROI are shown separated as a function of confidence and condition, illustrating dual effects in these regions (greater activity during Report and response to confidence during Report). Shaded areas reflect the SEM.

Figure 5.

Individual difference and connectivity analyses. The top panel illustrates the significant correlation between confidence-related activity in right rlPFC and metacognitive accuracy across subjects. The bottom panel depicts results of an exploratory psychophysiological interaction analysis (displayed at p < 0.001, uncorrected), revealing whole-brain corrected (p < 0.05) increases in connectivity between right rlPFC and visual cortex (lingual gyrus) and between right rlPFC and left dlPFC in Report compared to Follow trials.

Figure 6.

Analysis of right rlPFC activity using alternative GLMs (see Materials and Methods). A, Model 2 separated trials into correct and incorrect to assess whether error-related activity could account for effects of confidence. Parameter estimates (arbitrary units) are shown both for average activity during confidence rating (light gray) and the confidence parametric modulator (dark gray). Neither comparison revealed significant differences between correct and incorrect trials. B, Model 3 orthogonalized confidence with respect to reaction time, demonstrating that the effect of reported confidence remained after controlling for the variance in activity accounted for by RT. **p < 0.01; *p < 0.05. Error bars reflect the SEM.