Neuronal Correlates of Metacognition in Primate Frontal Cortex
Open accessAbstract
Humans are metacognitive: they monitor and control their cognition. Our hypothesis was that neuronal correlates of metacognition reside in the same brain areas responsible for cognition, including frontal cortex. Recent work demonstrated that nonhuman primates are capable of metacognition, so we recorded from single neurons in the frontal eye field, dorsolateral prefrontal cortex, and supplementary eye field of monkeys (Macaca mulatta) that performed a metacognitive visual-oculomotor task. The animals made a decision and reported it with a saccade, but received no immediate reward or feedback. Instead, they had to monitor their decision and bet whether it was correct. Activity was correlated with decisions and bets in all three brain areas, but putative metacognitive activity that linked decisions to appropriate bets occurred exclusively in the SEF. Our results offer a survey of neuronal correlates of metacognition and implicate the SEF in linking cognitive functions over short periods of time.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Postdecisional firing rates of neurons in prefrontal cortex and dopaminergic midbrain covary with choice correctness before explicit feedback is given.
“In animal models, postdecisional firing rates of neurons in prefrontal cortex and dopaminergic midbrain have also been shown to covary with choice correctness before explicit feedback is given (Kepecs et al. 2008, Middlebrooks & Sommer 2012, Tsujimoto et al. 2010).”
From Metacognition and Confidence: A Review and Synthesis (2024) · cites this paper as Middlebrooks & Sommer 2012
In Results > Single neuron recordings (page unavailable), postsaccade firing distinguished correct from incorrect choices in the supplementary eye field, a frontal cortical area. The same passage says prefrontal cortex showed no such postsaccade effect. This paper studied frontal cortical areas, not dopaminergic midbrain neurons, so it supports only a narrower version of the cited sentence. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Metacognition and cognitive monitoring: A new area of cognitive–developmental inquiry
Flavell, J. H. (1979) · American Psychologist · doi:10.1037/0003-066x.34.10.906 · Cited by 11,282 · cited 2× · see citing works
“To our knowledge the term “metacognition” was coined in the late 1970s (Flavell, 1976), and psychological frameworks have been developed to study and understand metacognitive processes (Flavell, 1979; Nelson and Narens, 1990).”
Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.2.331 · Cited by 2,685 · see citing works
Neural Basis of a Perceptual Decision in the Parietal Cortex (Area LIP) of the Rhesus Monkey
Shadlen, M. N., & Newsome, W. T. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.4.1916 · Cited by 1,755 · see citing works
Finding the self? An event-related fMRI study
Kelley, W. M., Macrae, C. N., Wyland, C. L., Caglar, S., Inati, S., & Heatherton, T. F. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/08989290260138672 · Cited by 1,606 · cited 1× · see citing works
“Like the metacognition studies, many self-referential processing studies report BOLD responses in medial prefrontal regions (Gusnard et al., 2001; Kelley et al., 2002; Macrae et al., 2004).”
Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex
Kiani, R., & Shadlen, M. N. (2009) · Science · doi:10.1126/science.1169405 · Cited by 1,027 · see citing works
Reward expectancy in primate prefrental neurons
Watanabe, M. (1996) · Nature · doi:10.1038/382629a0 · Cited by 684 · cited 1× · see citing works
“Each area has neuronal activity related to vision, saccades, and reward (Boch and Goldberg, 1989; Bruce and Goldberg, 1985; Ding and Hikosaka, 2006; Funahashi et al., 1991; Kim et al., 2008; Mohler et al., 1973; Roesch and Olson, 2003; Russo and Bruce, 1996; Stuphorn et al., 2000; Watanabe, 1996).”
Decision Making in Recurrent Neuronal Circuits
Wang, X.-J. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.034 · Cited by 679 · cited 1× · see citing works
“That idea is consistent with single neuron recordings in LIP (Kiani and Shadlen, 2009), and may be compatible with recurrent neuronal decision-making models (Wang, 2008).”
Differential attention-dependent response modulation across cell classes in macaque visual area V4
Mitchell, J. F., Sundberg, K. A., & Reynolds, J. H. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.018 · Cited by 665 · see citing works
Medial prefrontal activity predicts memory for self
Macrae, C. N. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh025 · Cited by 581 · cited 1× · see citing works
“Like the metacognition studies, many self-referential processing studies report BOLD responses in medial prefrontal regions (Gusnard et al., 2001; Kelley et al., 2002; Macrae et al., 2004).”
Rhesus monkeys know when they remember
Hampton, R. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.071600998 · Cited by 493 · see citing works
NEURAL SELECTION AND CONTROL OF VISUALLY GUIDED EYE MOVEMENTS
Schall, J. D., & Thompson, K. G. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.241 · Cited by 489 · see citing works
Transfer of metacognitive skills and hint seeking in monkeys
Kornell, N., Son, L. K., & Terrace, H. S. (2007) · Psychological Science · doi:10.1111/j.1467-9280.2007.01850.x · Cited by 341 · cited 6× · see citing works
“, 2004) seek information to improve future decisions, an example of metacognitive control, and rhesusmonkeys can be trained to bet whether a past decision was correct or incorrect, an example of metacognitive monitoring (Kornell et al., 2007).”
InfluentialMasson, M. E. J., & Rotello, C. M. (2009) · Journal of Experimental Psychology: Learning, Memory, and Cognition · doi:10.1037/a0014876 · Cited by 173 · see citing works
Neural Correlates for Feeling-of-Knowing
Kikyo, H., Ohki, K., & Miyashita, Y. (2002) · Neuron · doi:10.1016/s0896-6273(02)00939-x · Cited by 161 · see citing works
Flagged first, then by citations
Research works printed but not linked: 53
- Anderson EB Mitchell JF Reynolds JH 2011 Attentional modulation of firing rate varies with burstiness across putative pyramidal neurons in macaque visual area V4 J Neurosci 31 10983 10992 21795547 PMC3161825
- Barraclough DJ Conroy ML Lee D 2004 Prefrontal cortex and decision making in a mixed-strategy game Nat Neurosci 7 404 410 15004564
- Boch RA Goldberg ME 1989 Participation of prefrontal neurons in the preparation of visually guided eye movements in the rhesus monkey J Neurophysiol 61 1064 1084 2723730
- Bruce CJ Goldberg ME 1985 Primate frontal eye fields. I. Single neurons discharging before saccades J Neurophysiol 53 603 635 3981231
- Call J 2010 Do apes know that they could be wrong? Anim Cogn 13 689 700 20306102
- Chua EF Schacter DL Rand-Giovannetti E Sperling RA 2006 Understanding metamemory: neural correlates of the cognitive process and subjective level of confidence in recognition memory Neuroimage 29 1150 1160 16303318
- Connors BW Gutnick MJ 1990 Intrinsic firing patterns of diverse neocortical neurons Trends Neurosci 13 99 104 1691879
- Constantinidis C Goldman-Rakic PS 2002 Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex J Neurophysiol 88 3487 3497 12466463
- Crapse TB Sommer MA 2008 Corollary discharge across the animal kingdom Nat Rev Neurosci 9 587 600 18641666 PMC5153363
- Ding L Hikosaka O 2006 Comparison of reward modulation in the frontal eye field and caudate of the macaque J Neurosci 26 6695 6703 16793877 PMC6673837
- Foote AL Crystal JD 2007 Metacognition in the rat Curr Biol 17 551 555 17346969 PMC1861845
- Funahashi S Bruce CJ Goldman-Rakic PS 1990 Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms J Neurophysiol 63 814 831 2341879
- Funahashi S Bruce CJ Goldman-Rakic PS 1991 Neuronal activity related to saccadic eye movements in the monkey’s dorsolateral prefrontal cortex J Neurophysiol 65 1464 1483 1875255
- Hampton RR Zivin A Murray EA 2004 Rhesus monkeys (Macaca mulatta) discriminate between knowing and not knowing and collect information as needed before acting Anim Cogn 7 239 246 15105996
- Iba M Sawaguchi T 2003 Involvement of the dorsolateral prefrontal cortex of monkeys in visuospatial target selection J Neurophysiol 89 587 599 12522204
- Johnston K Everling S 2006 Neural activity in monkey prefrontal cortex is modulated by task context and behavioral instruction during delayed-match-to-sample and conditional prosaccade-antisaccade tasks J Cogn Neurosci 18 749 765 16768375
- Kepecs A Uchida N Zariwala HA Mainen ZF 2008 Neural correlates, computation and behavioural impact of decision confidence Nature 455 227 231 18690210
- Kim JN Shadlen MN 1999 Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque Nat Neurosci 2 176 185 10195203
- Kim S Hwang J Lee D 2008 Prefrontal coding of temporally discounted values during intertemporal choice Neuron 59 161 172 18614037 PMC2593737
- Mays LE Sparks DL 1980 Saccades are spatially, not retinocentrically, coded Science 208 1163 1165 6769161
- McCoy AN Platt ML 2005 Expectations and outcomes: decision-making in the primate brain J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191 201 211 15759141
- Middlebrooks PG Sommer MA 2011 Metacognition in monkeys during an oculomotor task J Exp Psychol Learn Mem Cogn 37 325 337 21171807 PMC3649877
- Miller EK Cohen JD 2001 An integrative theory of prefrontal cortex function Annu Rev Neurosci 24 167 202 11283309
- Mohler CW Goldberg ME Wurtz RH 1973 Visual receptive fields of frontal eye field neurons Brain Res 61 385 389 4204128
- Nakamura K Roesch MR Olson CR 2005 Neuronal activity in macaque SEF and ACC during performance of tasks involving conflict J Neurophysiol 93 884 908 15295008
- Pannu JK Kaszniak AW Rapcsak SZ 2005 Metamemory for faces following frontal lobe damage J Int Neuropsych Soc 11 668 676 16248902
- Pouget P Emeric EE Stuphorn V Reis K Schall JD 2005 Chronometry of visual responses in frontal eye field, supplementary eye field, and anterior cingulate cortex J Neurophysiol 94 2086 2092 15944228
- Roesch MR Olson CR 2003 Impact of expected reward on neuronal activity in prefrontal cortex, frontal and supplementary eye fields and premotor cortex J Neurophysiol 90 1766 1789 12801905
- Romanski LM 2004 Domain specificity in the primate prefrontal cortex Cogn Affect Behav Neurosci 4 421 429 15849888
- Rounis E Maniscalco B Rothwell JC Passingham RE Lau H 2010 Theta-burst transcranial magnetic stimulation to the prefrontal cortex impairs metacognitive visual awareness Cogn Neurosci 1 165 175 24168333
- Russo GS Bruce CJ 1996 Neurons in the supplementary eye field of rhesus monkeys code visual targets and saccadic eye movements in an oculocentric coordinate system J Neurophysiol 76 825 848 8871203
- Sato TR Schall JD 2003 Effects of stimulus-response compatibility on neural selection in frontal eye field Neuron 38 637 648 12765614
- Schall JD 2001 Neural basis of deciding, choosing and acting Nat Rev Neurosci 2 33 42 11253357
- Schall JD Hanes DP Thompson KG King DJ 1995 Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation J Neurosci 15 6905 6918 7472447 PMC6577995
- Schlag J Schlag-Rey M 1987 Evidence for a supplementary eye field J Neurophysiol 57 179 200 3559671
- Schnyer DM Verfaellie M Alexander MP LaFleche G Nicholls L Kaszniak AW 2004 A role for right medial prefontal cortex in accurate feeling-of-knowing judgements: evidence from patients with lesions to frontal cortex Neuropsychologia 42 957 966 14998710
- Seo H Lee D 2009 Behavioral and neural changes after gains and losses of conditioned reinforcers J Neurosci 29 3627 3641 19295166 PMC2750005
- Shields WE Smith JD Guttmannova K Washburn DA 2005 Confidence judgments by humans and rhesus monkeys J Gen Psychol 132 165 186 15871299 PMC4607308
- Smith JD Schull J Strote J McGee K Egnor R Erb L 1995 The uncertain response in the bottlenosed dolphin (Tursiops truncatus) J Exp Psychol Gen 124 391 408 8530911
- Smith JD Shields WE Allendoerfer KR Washburn DA 1998 Memory monitoring by animals and humans J Exp Psychol Gen 127 227 250 9742715
- So NY Stuphorn V 2010 Supplementary eye field encodes option and action value for saccades with variable reward J Neurophysiol 104 2634 2653 20739596 PMC4073903
- So NY Stuphorn V 2012 Supplementary eye field encodes reward prediction error J Neurosci 32 2950 2963 22378869 PMC3296227
- Sommer MA Wurtz RH 2000 Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus J Neurophysiol 83 1979 2001 10758109
- Sommer MA Wurtz RH 2001 Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus J Neurophysiol 85 1673 1685 11287490
- Sommer MA Wurtz RH 2004 What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus J Neurophysiol 91 1381 1402 14573558
- Stuphorn V Taylor TL Schall JD 2000 Performance monitoring by the supplementary eye field Nature 408 857 860 11130724
- Suda-King C 2008 Do orangutans (Pongo pygmaeus) know when they do not remember? Anim Cogn 11 21 42 17437141
- Sutton RS Barto AG 1998 Reinforcement learning 9 Cambridge, MA MIT Press
- Tanji J Hoshi E 2008 Role of the lateral prefrontal cortex in executive behavioral control Physiol Rev 88 37 57 18195082
- Thompson KG Bichot NP 2005 A visual salience map in the primate frontal eye field Prog Brain Res 147 251 262 15581711
- Thompson KG Schall JD 1999 The detection of visual signals by macaque frontal eye field during masking Nat Neurosci 2 283 288 10195223
- Wallis JD Miller EK 2003 From rule to response: neuronal processes in the premotor and prefrontal cortex J Neurophysiol 90 1790 1806 12736235
- Zar JH 1999 Biostatistical Analysis New Jersey Prentice Hall
Cited by
Sorted by citations
Confidence and certainty: Distinct probabilistic quantities for different goals
Pouget, A., Drugowitsch, J., & Kepecs, A. (2016) · Nature Neuroscience · doi:10.1038/nn.4240 · Cited by 528 · see citing works
Choice Certainty Is Informed by Both Evidence and Decision Time
Kiani, R., Corthell, L., & Shadlen, M. N. (2014) · Neuron · doi:10.1016/j.neuron.2014.12.015 · Cited by 470 · see citing works
Confidence as Bayesian probability: From neural origins to behavior
Meyniel, F., Sigman, M., & Mainen, Z. F. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.039 · Cited by 349 · see citing works
Neural Coding of Uncertainty and Probability
Ma, W. J., & Jazayeri, M. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071013-014017 · Cited by 290 · see citing works
Metacognition and Confidence: A Review and Synthesis
Fleming, S. M. (2024) · Annual Review of Psychology · doi:10.1146/annurev-psych-022423-032425 · Cited by 256 · see citing works
Distinct encoding of decision confidence in human medial prefrontal cortex
Bang, D., & Fleming, S. M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800795115 · Cited by 207 · see citing works
Fouragnan, E., Retzler, C., & Philiastides, M. G. (2018) · Human Brain Mapping · doi:10.1002/hbm.24047 · Cited by 176 · see citing works
Individual consistency in the accuracy and distribution of confidence judgments
Ais, J., Zylberberg, A., Barttfeld, P., & Sigman, M. (2016) · Cognition · doi:10.1016/j.cognition.2015.10.006 · Cited by 174 · see citing works
The neural system of metacognition accompanying decision-making in the prefrontal cortex
Qiu, L., Su, J., Ni, Y., Bai, Y., Zhang, X., Li, X., & Wan, X. (2018) · PLOS Biology · doi:10.1371/journal.pbio.2004037 · Cited by 125 · see citing works
Causal neural network of metamemory for retrospection in primates
Miyamoto, K., Osada, T., Setsuie, R., Takeda, M., Tamura, K., Adachi, Y., & Miyashita, Y. (2017) · Science · doi:10.1126/science.aal0162 · Cited by 106 · see citing works
Behavior- and Modality-General Representation of Confidence in Orbitofrontal Cortex
Masset, P., Ott, T., Lak, A., Hirokawa, J., & Kepecs, A. (2020) · Cell · doi:10.1016/j.cell.2020.05.022 · Cited by 109 · see citing works
Understanding neural signals of post-decisional performance monitoring: An integrative review
Desender, K., Ridderinkhof, K. R., & Murphy, P. R. (2021) · eLife · doi:10.7554/elife.67556 · Cited by 77 · see citing works
Khalvati, K., Kiani, R., & Rao, R. P. N. (2021) · Nature Communications · doi:10.1038/s41467-021-25419-4 · Cited by 64 · see citing works
Studying the neural representations of uncertainty
Walker, E. Y., Pohl, S., Denison, R. N., Barack, D. L., Lee, J., Block, N., Ma, W. J., & Meyniel, F. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01444-y · Cited by 56 · see citing works
Yeon, J., Shekhar, M., & Rahnev, D. (2020) · Scientific Reports · doi:10.1038/s41598-020-77820-6 · Cited by 30 · see citing works
Miyamoto, K., Harbison, C., Tanaka, S., Saito, M., Luo, S., Matsui, S., Sankhe, P., Mahmoodi, A., Lin, M., Trudel, N., et al. (2025) · Nature Communications · doi:10.1038/s41467-024-55202-0 · Cited by 4 · see citing works
- Authors
- Middlebrooks, P. G., & Sommer, M. A.
- Affiliations
- University of Pittsburgh (US)
- Corresponding author
- Middlebrooks, Paul G.
- ORCID
- Sommer, Marc A.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-08
- Volume
- 75
- Issue
- 3
- Pages
- 517-530
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3418516
- OpenAlex
- W2064259685
- Cited by
- 124
- References
- 14
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 8 · 2023: 8 · 2022: 4 · 2021: 10 · 2020: 10 · 2019: 8 · 2018: 16 · 2017: 9 · 2016: 6 · 2015: 10 · 2014: 15 · 2013: 6 · 2012: 1
- FWCI
- 4.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- D-Scholarship@Pitt (University of Pittsburgh) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
- Funders
- National Institute of Mental Health (F31MH087094)
- National Eye Institute (EY-017592, R01EY017592)
- National Institute of Biomedical Imaging and Bioengineering (P41EB001977)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- metacognition, neural correlates, supplementary eye field, dorsolateral prefrontal cortex, frontal eye field, non-human primates, saccades, single-unit recording, rhesus monkeys
- MeSH terms
- Animals, Cognition, Electrophysiology, Frontal Lobe, Macaca mulatta, Male, Neurons, Psychomotor Performance
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
