Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex
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Abstract
ABSTRACT The human prefrontal cortex (PFC) has been associated more with meta-perceptual as opposed to meta-memory decisions from correlational neuroimaging investigations. Recently, metacognitive abilities have also been shown to be causally dependent upon anterior and dorsal PFC in non-human primate lesion studies. Two studies, utilizing post-decision wagering paradigms and reversible inactivation, challenged this meta-perceptual versus meta-memory notion and showed that dorsal and anterior prefrontal areas are associated with metamemory for experienced objects and awareness of ignorance respectively. Causal investigations are important but scarce; nothing is known, for example, about the causal contributions of prefrontal sub-regions to spatial metamemory. Here, we investigated the effects of dorsal versus ventral PFC lesions on two-alternative forced choice spatial discrimination tasks in male macaque monkeys. Importantly, we were rigorous in approach and applied three independent but complementary indices used to quantify individual animals’ metacognitive ability (“type II sensitivity”) namely meta-d′, d ′ measures, and Phi coefficient (Φ). Our results were consistent across indices: while neither lesions to superior dorsolateral PFC (sdlPFC) nor orbitofrontal cortex (OFC) impaired spatial recognition performance, only monkeys with sdlPFC lesions were impaired in meta-accuracy. Together with the observation that the same OFC lesioned monkeys were impaired in updating rule-value in a Wisconsin Card Sorting Test analog, we therefore document a functional double-dissociation between these two PFC regions. Out study presents important causal evidence that other dimensions, namely domain-specific processing (e.g., spatial versus non-spatial metamemory), also need considerations in understanding the functional specialization in the neural underpinnings of introspection. Significance Statement This study demonstrates macaque monkeys’ meta-cognitive capability of introspecting its own memory success is causally dependent on intact superior dorsolateral prefrontal cortices (PFC) but not the orbitofrontal cortices. Combining neurosurgical techniques on monkeys and state-of-the-art measures of metacognition, we affirm a critical role of the PFC in supporting spatial meta-recognition memory and delineate functional specificity within PFC for distinct elements of metacognition.
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Changes in confidence formation and metacognition (but not first-order task performance) are observed following temporary disruption or lesions to rostrolateral prefrontal cortex (Brodmann areas 46 and 10) in humans and monkeys.
“Changes in confidence formation and metacognition (but not first-order task performance) are observed following temporary disruption or lesions to rostrolateral prefrontal cortex (Brodmann areas 46 and 10) in humans and monkeys (Fleming et al. 2014;Kwok et al. 2019;Miyamoto et al. 2017Miyamoto et al. , 2018;;Shekhar & Rahnev 2018)”
From Metacognition and Confidence: A Review and Synthesis (2024) · cites this paper as Kwok et al. 2019
The Discussion reports that superior dorsolateral prefrontal lesions impaired macaques’ spatial metamemory without impairing first-order spatial recognition. The Materials and Methods specify lesions involving lateral area 9 and dorsal portions of areas 46 and 9/46, but explicitly excluding area 10. This study therefore supports the macaque lesion finding, not the sentence’s broader framing around areas 46 and 10 in humans and monkeys. (LLM, conf=0.86)
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- Authors
- Kwok, S. C., Cai, Y., & Buckley, M. J.
- Affiliations
- New York University Shanghai (CN)
- East China Normal University (CN)
- University of Oxford (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2019-05-23
- Volume
- 39
- Issue
- 30
- Pages
- 5922-5934
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6650985
- OpenAlex
- W2952690096
- Cited by
- 28
- References
- 63
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 8 · 2021: 5 · 2020: 3
- FWCI
- 2.33
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Natural Science Foundation of Shanghai (16ZR1410200)
- New York University Shanghai
- Wellcome Trust (101092/Z/13/Z)
- Science and Technology Commission of Shanghai Municipality
- East China Normal University
- Medical Research Council (MR/K005480/1)
- RIKEN
- Fundamental Research Funds for the Central Universities (2018ECNU-HWFW007)
- NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai
- RIKEN Brain Science Institute
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- metacognition, metamemory, self-reflection, dorsolateral prefrontal cortex, orbitofrontal cortex, spatial recognition memory, macaque, lesion studies, double dissociation, phi coefficient, Wisconsin Card Sorting Test, rule updating
- MeSH terms
- Metacognition, Macaca fuscata, Animals, Choice Behavior, Discrimination, Psychological, Macaca fascicularis, Macaca mulatta, Male, Reaction Time, Prefrontal Cortex, Spatial Processing
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 ›
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