Prefrontal Contributions to Metacognition in Perceptual Decision Making

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.

[1]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[2]  Bryan Rodgers,et al.  What does a Man do after he Makes an Error? An Analysis of Response Programming , 1977 .

[3]  S. Michael Malinconico,et al.  Decisions under Uncertainty. , 1984 .

[4]  T. O. Nelson Metamemory: A Theoretical Framework and New Findings , 1990 .

[5]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[6]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[7]  Nigel Harvey,et al.  Confidence in judgment , 1997, Trends in Cognitive Sciences.

[8]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[9]  T. Shallice,et al.  Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval , 2000, Journal of Cognitive Neuroscience.

[10]  H. Pashler,et al.  Confidence and Accuracy of Near-Threshold Discrimination Responses , 2001, Consciousness and Cognition.

[11]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

[12]  K. R. Ridderinkhof,et al.  Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. , 2001, Psychophysiology.

[13]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[14]  Susan J. Galvin,et al.  Type 2 tasks in the theory of signal detectability: Discrimination between correct and incorrect decisions , 2003, Psychonomic bulletin & review.

[15]  Timothy D. Wilson,et al.  Self-knowledge: its limits, value, and potential for improvement. , 2004, Annual review of psychology.

[16]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[17]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[18]  A. Beck,et al.  A new instrument for measuring insight: the Beck Cognitive Insight Scale , 2004, Schizophrenia Research.

[19]  M. Alexander,et al.  A role for right medial prefrontal cortex in accurate feeling-of-knowing judgments: evidence from patients with lesions to frontal cortex , 2004, Neuropsychologia.

[20]  Neil A. Macmillan,et al.  Detection theory: A user's guide, 2nd ed. , 2005 .

[21]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[22]  G. McCarthy,et al.  Decisions under Uncertainty: Probabilistic Context Influences Activation of Prefrontal and Parietal Cortices , 2005, The Journal of Neuroscience.

[23]  Alfred W. Kaszniak,et al.  Metamemory Experiments in Neurological Populations: A Review , 2005, Neuropsychology Review.

[24]  John D E Gabrieli,et al.  Neural correlates of actual and predicted memory formation , 2005, Nature Neuroscience.

[25]  Petter Johansson,et al.  Failure to Detect Mismatches Between Intention and Outcome in a Simple Decision Task , 2005, Science.

[26]  R. Cabeza,et al.  Cerebral Cortex doi:10.1093/cercor/bhj097 Role of Prefrontal and Anterior Cingulate Regions in Decision-Making Processes Shared by Memory and Nonmemory Tasks , 2005 .

[27]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[28]  Sterling C. Johnson,et al.  Neural correlates of self-evaluative accuracy after traumatic brain injury , 2006, Neuropsychologia.

[29]  D. Kornbrot,et al.  Signal detection theory, the approach of choice: Model-based and distribution-free measures and evaluation , 2006, Perception & psychophysics.

[30]  A. Cowey,et al.  Post-decision wagering objectively measures awareness , 2007, Nature Neuroscience.

[31]  Hongkeun Kim,et al.  Trusting Our Memories: Dissociating the Neural Correlates of Confidence in Veridical versus Illusory Memories , 2007, The Journal of Neuroscience.

[32]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[33]  Hatim A. Zariwala,et al.  Neural correlates, computation and behavioural impact of decision confidence , 2008, Nature.

[34]  Jan Gläscher,et al.  Visualization of Group Inference Data in Functional Neuroimaging , 2009, Neuroinformatics.

[35]  K. R. Ridderinkhof,et al.  Frontal Cortex Mediates Unconsciously Triggered Inhibitory Control , 2008, The Journal of Neuroscience.

[36]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[37]  Daniel L. Schacter,et al.  Neural Correlates of Metamemory: A Comparison of Feeling-of-Knowing and Retrospective Confidence Judgments , 2009, Journal of Cognitive Neuroscience.

[38]  M. Shadlen,et al.  Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex , 2009, Science.

[39]  M. Conrad,et al.  On the functional nature of the N400: Contrasting effects related to visual word recognition and contextual semantic integration , 2010, Cognitive neuroscience.

[40]  P. Berkes,et al.  Statistically Optimal Perception and Learning: from Behavior to Neural Representations , 2022 .

[41]  M. Sahani,et al.  Effects of Category-Specific Costs on Neural Systems for Perceptual Decision-Making , 2010, Journal of neurophysiology.

[42]  Gustavo Deco,et al.  Choice, difficulty, and confidence in the brain , 2010, NeuroImage.

[43]  John Duncan,et al.  Executive function and fluid intelligence after frontal lobe lesions , 2009, Brain : a journal of neurology.

[44]  R. Passingham,et al.  Theta-burst transcranial magnetic stimulation to the prefrontal cortex impairs metacognitive visual awareness , 2010, Cognitive neuroscience.

[45]  R. Kawashima,et al.  Right frontopolar cortex activity correlates with reliability of retrospective rating of confidence in short-term recognition memory performance , 2010, Neuroscience Research.

[46]  P. Latham,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S11 References Movie S1 Optimally Interacting Minds R�ports , 2022 .

[47]  Geraint Rees,et al.  Relating Introspective Accuracy to Individual Differences in Brain Structure , 2010, Science.

[48]  E. Rolls,et al.  Confidence-related decision making. , 2010, Journal of neurophysiology.

[49]  Timothy J. Pleskac,et al.  Two-stage dynamic signal detection: a theory of choice, decision time, and confidence. , 2010, Psychological review.

[50]  Gordon D Logan,et al.  Cognitive Illusions of Authorship Reveal Hierarchical Error Detection in Skilled Typists , 2010, Science.

[51]  Aldo Genovesio,et al.  Evaluating self-generated decisions in frontal pole cortex of monkeys , 2009, Nature Neuroscience.

[52]  Irene Liu,et al.  Improved modulation of rostrolateral prefrontal cortex using real-time fMRI training and meta-cognitive awareness , 2011, NeuroImage.

[53]  Raymond J. Dolan,et al.  Deconstructing risk: Separable encoding of variance and skewness in the brain , 2011, NeuroImage.

[54]  Zara M. Bergström,et al.  A Specific Brain Structural Basis for Individual Differences in Reality Monitoring , 2011, The Journal of Neuroscience.

[55]  D. Schwarzkopf,et al.  Relating inter-individual differences in metacognitive performance on different perceptual tasks , 2011, Consciousness and Cognition.

[56]  Paul M. Grant,et al.  Assessment of cognitive insight: a qualitative review. , 2012, Schizophrenia bulletin.

[57]  R. Dolan,et al.  The neural basis of metacognitive ability , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[58]  Adam Kepecs,et al.  A computational framework for the study of confidence in humans and animals , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[59]  Jessica R. Andrews-Hanna,et al.  The Brain’s Default Network and Its Adaptive Role in Internal Mentation , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[60]  H. Lau,et al.  A signal detection theoretic approach for estimating metacognitive sensitivity from confidence ratings , 2012, Consciousness and Cognition.

[61]  C. Frith,et al.  Mechanisms of social cognition. , 2012, Annual review of psychology.

[62]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .