Domain-General and Domain-Specific Patterns of Activity Supporting Metacognition in Human Prefrontal Cortex

Abstract

Metacognition is the capacity to evaluate the success of one's own cognitive processes in various domains, e.g. memory and perception. It remains controversial whether metacognition relies on a domain-general resource that is applied to different tasks, or whether self-evaluative processes are domain-specific. Here we directly investigated this issue by examining the neural substrates engaged when metacognitive judgments were made during perceptual and memory tasks matched for stimulus and performance characteristics. By comparing patterns of functional magnetic resonance imaging (fMRI) activity while subjects evaluated their performance, we revealed both domain-specific and domain-general metacognitive representations. Multi-voxel activity patterns in right frontopolar cortex predicted levels of confidence in a domain-specific fashion, whereas domain-general signals predicting confidence and accuracy were found in a widespread network in the frontal and posterior midline. Moreover, individual differences in perceptual and memory metacognitive ability were predicted by the degree of confidence decoding in frontal and parietal cortex, respectively. The demonstration of domain-specific metacognitive representations suggests the presence of a content-rich mechanism available to introspection and cognitive control. Major subject area: Neuroscience 2Metacognition is the capacity to evaluate the success of one's cognitive processes in various do-3 mains, e.g. perception or memory (1-4). Metacognitive ability can be assessed in the laboratory 4 by quantifying the trial-by-trial correspondence between objective performance and subjective 5 confidence (5-8). Anatomical (9-11), functional (12-16) and neuropsychological (1-4,17-19) evi-6 dence indicates specific neural substrates (especially in frontolateral, frontomedial, and parietal 7 regions) contribute to metacognition across a range of task domains, including memory and per-8 ception. However, the neurocognitive architecture supporting metacognition remains controver-9 sial. Does metacognition rely on a common, domain-general resource that is recruited to evaluate 10 performance on a variety of tasks? Or is metacognition supported by domain-specific compo-11 nents? 12Current computational perspectives (20,21) suggest both domain-general and domain-13 specific representations may be important for guiding behavior. On the one hand, one needs to be 14 able to compare confidence estimates in a "common currency" across a range of arbitrary deci-15 sion scenarios (22). One solution to this problem is to maintain a global resource with access to 16 arbitrary sensorimotor mappings (23-25). Candidate neural substrates for a domain-general re-17 source are the frontoparietal and cingulo-opercular networks, known to be involved in arbitrary 18 control operations (23). In particular, the dorsomedial prefrontal cortex (dmPFC; encompassing 19 the paracingulate cortex and pre-supplementary motor area) has been implicated both in repre-20 senting confidence and detecting errors acros...

Disruptions of frontoparietal control network and default mode network linking the metacognitive deficits with clinical symptoms in schizophrenia

“…The newly involving fMRI activities during the redecision phase in comparison to those during the first decision‐making phase are not necessarily related to metacognition, could be generally associated with the second decision‐making. However, the fMRI activities in the MCN predominately occurring during the redecision phase were subject to the decision uncertainty levels on the preceding decisions, similar to the findings in the previous studies (Fleming et al, ; Morales et al, ; Qiu et al, ; Wan et al, ). Specifically, we here found that metacognitive abilities of decision uncertainty monitoring were lower, and the strengths of fMRI activities in the MCN, especially in dACC, were consistently much more reduced in SZ than HC.…”

“…The trial‐by‐trial neural activity (n‐ AUC ) quantitatively characterized the individual metacognitive ability of decision uncertainty monitoring (b‐ AUC ), underlying the metacognitive deficit in SZ. As the MCN is commonly associated with metacognition accompanying a variety of decision‐making tasks (Fleming et al, ; Morales et al, ; Qiu et al, ; Wan et al, ), the association of hypo‐activity in the MCN with the metacognitive deficit in SZ could be general. The hypo‐activity in the MCN was consistent with the replicated findings of structural and functional abnormalities in this network in SZ (Brugger & Howes, ; Carter et al, ; Goodkind et al, ; Kerns et al, ; Pettersson‐Yeo et al, ).…”

“…Although there have existed many clinical studies on the metacognitive deficits in SZ, a lack of operational definition of metacognitive deficits makes it difficult to use a proper experimental paradigm to investigate the underlying neural mechanisms. To date, there are growing interests in neuroscience to investigate neural mechanisms of metacognition (Fleming, Huijgen, & Dolan, ; Kiani & Shadlen, ; Miyamoto et al, ; Morales, Lau, & Fleming, ). Nevertheless, the neural accounts linking the metacognitive deficits and clinical symptoms in SZ remain largely obscure (Buchy, Stowkowy, MacMaster, Nyman, & Addington, ; Francis et al, ).…”

“…In contrast, when the decision uncertainty is high, the metacognitive processes should be evoked to revise the preceding decision. Several recent studies using functional MRI (fMRI) in simple perceptual decision‐making tasks have shown that the frontoparietal control network (FPCN) and the salience network (SN) are associated with metacognition accompanying the decision‐making task in the population of HC (Fleming et al, ; Morales et al, ; Qiu et al, ; Wan, Cheng, & Tanaka, ). The fMRI activities in these regions increase as decision uncertainty increases.…”

Believing is representation mediated by the dopamine brain system

“…Third, the data of Babayan et al. () concur with the finding that perceptual and memory‐specific metacognitive representations coexist with generic confidence signals (Morales, Lau, & Fleming, ). In fact, activity in the anterior prefrontal cortex was reported to predict levels of confidence in a domain‐specific fashion, whereas domain‐general signals predicted confidence and accuracy in frontal and parietal midline areas.…”