Medial and lateral networks in anterior prefrontal cortex support metacognitive ability for memory and perception

Abstract

Convergent evidence indicates that frontopolar Brodmann area 10, and more generally the anterior prefrontal cortex (aPFC), supports the human capacity to monitor and reflect on cognition and experience. An important unanswered question, however, is whether aPFC is a homogeneous region that supports a general-purpose metacognitive ability or whether there could be regional specialization within aPFC with respect to specific types of metacognitive processes. Previous studies suggest that the lateral and medial subdivisions within aPFC may support metacognitive judgments of moment-to-moment perceptual processes and assessments of information from memory stored over longer time scales, respectively. Here we directly compared intraindividual variability in metacognitive capacity for perceptual decisions and memorial judgments and used resting-state functional connectivity (rs-fcMRI) to relate this variability to the connectivity of the medial and lateral regions of aPFC. We found a behavioral dissociation in metacognitive ability for perceptual and memorial judgments. Furthermore, functional connectivity analysis revealed distinct patterns of connectivity that correlated with individual differences in each domain. Metacognitive ability for perceptual decisions was associated with greater connectivity between lateral regions of aPFC and right dorsal anterior cingulate cortex, bilateral putamen, right caudate, and thalamus, whereas metacognitive ability for memory retrieval predicted greater connectivity between medial aPFC and the right central precuneus and intraparietal sulcus/inferior parietal lobule. Together, these results suggest that an individual's capacity for accurate introspection in the domains of perception and memory is related to the functional integrity of unique neural networks anchored in the medial and lateral regions of the aPFC.

Figure 1.

Experimental paradigm. Participants completed 2 tasks in a counterbalanced order. A, Perceptual discrimination task. Each trial (N = 360) consisted of a visual display of 6 Gabor gratings, followed by an ISI of 500 ms, followed by a second visual display of 6 Gabor gratings. In one of the two displays, the orientation of one randomly selected Gabor patch was tilted slightly from the vertical axis. The orientation angle of this pop-out Gabor was adjusted using a 2-up 1-down adaptive staircase procedure. Participants made unspeeded 2-choice discrimination judgments as to whether the “pop-out” Gabor occurred in either the first or second stimulus display, then rated their confidence in the accuracy of their response on a scale of 1 (low confidence) to 6 (high confidence). B, Memory retrieval task. The memory task consisted of a classic verbal recognition memory paradigm. During encoding, participants viewed 145 words randomly selected from a set of 290 words. During recognition, participants were presented with each word from the full list of stimuli in a random order (half of which were presented during encoding and half of which were new) and were asked to make unspeeded 2-choice discrimination judgments as to whether the stimulus was old or new, and then rated their confidence in their response.

Figure 2.

Behavioral results. Scatterplot of zero-order correlation between metacognitive accuracy for perceptual decisions (A_roc) and memorial judgments (M_ratio) [r(50) = 0.03, p = 0.81].

Figure 3.

A, Lateral aPFC connectivity. Right lateral aPFC showed intrinsic connectivity with a broad network, including bilateral regions of superior frontal gyrus, cingulate gyrus, inferior frontal gyrus, precuneus, postcentral gyrus, inferior parietal lobule, lateral temporal cortex, orbital frontal cortex, thalamus, basal ganglia, caudate, insula, and cerebellum. B, Medial aPFC connectivity. Right medial aPFC displayed connectivity with bilateral regions of medial prefrontal cortex, orbital frontal cortex, precuneus, inferior parietal lobule, lateral temporal cortex, precentral gyrus, posterior and anterior cingulate, hippocampal formation, insula, thalamus, inferior occipital gyrus, and cerebellum.

Figure 4.

A, Seed regions. To estimate connectivity, two spherical ROIs of 6 mm diameter with centers at 6, 58, 0 (medial aPFC; reflecting the area described by Gilbert et al., 2006; meta-analysis) and 24, 58, 18 (lateral aPFC; reflecting the area reported by Fleming et al. (2010)) were defined in MNI152 space. B, fMRI connectivity results. Top two panels, Metacognitive accuracy for perceptual decisions is associated with increased connectivity between lateral aPFC seed region and right dACC, bilateral putamen, right caudate, and thalamus. Bottom two panels, Metacognitive accuracy for memory is associated with increased connectivity between medial aPFC and right precuneus and right IPS/IPL. All clusters are significant at p < 0.05, corrected for multiple comparisons using topological FDR (cluster forming threshold, p < 0.005). C, Correlation between metacognitive accuracy scores and mean normalized correlation values of significant clusters.

Figure 5.

Differential functional connectivity between medial and lateral aPFC correlated with metacognitive accuracy for memory. A, Medial aPFC–lateral aPFC connectivity correlated with metacognitive accuracy for memory predicted 5 clusters, including the hippocampal formation, precuneus, fusiform gyrus, lingual gyrus, and precentral gyrus (Table 2). All clusters are significant at p < 0.05, corrected for multiple comparisons using topological FDR (cluster forming threshold, p < 0.005). B, Correlation between metacognitive accuracy scores and mean normalized correlation values of medial–lateral aPFC functional connectivity of all significant clusters.