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Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex.
J Neurosci. 2019 07 24; 39(30):5922-5934.JN

Abstract

The human 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 nonhuman primate lesion studies. Two studies, using postdecision 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 subregions 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") by two variants of meta-d'/d' and phi coefficient (φ). Our results were consistent across indices: while neither lesions to superior dorsolateral PFC nor orbitofrontal cortex impaired spatial recognition performance, only monkeys with superior dorsolateral PFC lesions were impaired in meta-accuracy. Together with the observation that the same orbitofrontal cortex 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. Our study presents important causal evidence that other dimensions, namely, domain-specific processing (e.g., spatial vs nonspatial metamemory), also need considerations in understanding the functional specialization in the neural underpinnings of introspection.SIGNIFICANCE STATEMENT This study demonstrates macaque monkeys' metacognitive capability of introspecting its own memory success is causally dependent on intact superior dorsolateral prefrontal cortices 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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Authors+Show Affiliations

Kwok SC
Shanghai Key Laboratory of Brain Functional Genomics, Key Laboratory of Brain Functional Genomics Ministry of Education, School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China, sze-chai.kwok@st-hughs.oxon.org. Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai 200062, China. NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China, and.
Cai Y
Shanghai Key Laboratory of Brain Functional Genomics, Key Laboratory of Brain Functional Genomics Ministry of Education, School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China.
Buckley MJ
Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, United Kingdom.

MeSH

AnimalsChoice BehaviorDiscrimination, PsychologicalMacaca fascicularisMacaca fuscataMacaca mulattaMaleMetacognitionPrefrontal CortexReaction TimeSpatial Processing

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

31123101

Citation

Kwok, Sze Chai, et al. "Mnemonic Introspection in Macaques Is Dependent On Superior Dorsolateral Prefrontal Cortex but Not Orbitofrontal Cortex." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 39, no. 30, 2019, pp. 5922-5934.
Kwok SC, Cai Y, Buckley MJ. Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex. J Neurosci. 2019;39(30):5922-5934.
Kwok, S. C., Cai, Y., & Buckley, M. J. (2019). Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 39(30), 5922-5934. https://doi.org/10.1523/JNEUROSCI.0330-19.2019
Kwok SC, Cai Y, Buckley MJ. Mnemonic Introspection in Macaques Is Dependent On Superior Dorsolateral Prefrontal Cortex but Not Orbitofrontal Cortex. J Neurosci. 2019 07 24;39(30):5922-5934. PubMed PMID: 31123101.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex. AU - Kwok,Sze Chai, AU - Cai,Yudian, AU - Buckley,Mark J, Y1 - 2019/05/23/ PY - 2019/02/08/received PY - 2019/05/06/revised PY - 2019/05/07/accepted PY - 2019/5/28/pubmed PY - 2020/6/18/medline PY - 2019/5/25/entrez KW - introspection KW - lesion KW - macaques KW - metacognition KW - prefrontal cortex KW - recognition memory SP - 5922 EP - 5934 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J Neurosci VL - 39 IS - 30 N2 - The human 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 nonhuman primate lesion studies. Two studies, using postdecision 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 subregions 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") by two variants of meta-d'/d' and phi coefficient (φ). Our results were consistent across indices: while neither lesions to superior dorsolateral PFC nor orbitofrontal cortex impaired spatial recognition performance, only monkeys with superior dorsolateral PFC lesions were impaired in meta-accuracy. Together with the observation that the same orbitofrontal cortex 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. Our study presents important causal evidence that other dimensions, namely, domain-specific processing (e.g., spatial vs nonspatial metamemory), also need considerations in understanding the functional specialization in the neural underpinnings of introspection.SIGNIFICANCE STATEMENT This study demonstrates macaque monkeys' metacognitive capability of introspecting its own memory success is causally dependent on intact superior dorsolateral prefrontal cortices 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. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/31123101/Mnemonic_Introspection_in_Macaques_Is_Dependent_on_Superior_Dorsolateral_Prefrontal_Cortex_But_Not_Orbitofrontal_Cortex_ DB - PRIME DP - Unbound Medicine ER -