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Research Articles, Behavioral/Cognitive

Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex

Sze Chai Kwok (郭思齊), Yudian Cai (蔡禹甸) and Mark J. Buckley
Journal of Neuroscience 24 July 2019, 39 (30) 5922-5934; DOI: https://doi.org/10.1523/JNEUROSCI.0330-19.2019
Sze Chai Kwok (郭思齊)
1Shanghai 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,
2Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai 200062, China,
3NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China, and
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Yudian Cai (蔡禹甸)
1Shanghai 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,
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Mark J. Buckley
4Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, United Kingdom
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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.

  • introspection
  • lesion
  • macaques
  • metacognition
  • prefrontal cortex
  • recognition memory

This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The Journal of Neuroscience: 39 (30)
Journal of Neuroscience
Vol. 39, Issue 30
24 Jul 2019
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Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex
Sze Chai Kwok (郭思齊), Yudian Cai (蔡禹甸), Mark J. Buckley
Journal of Neuroscience 24 July 2019, 39 (30) 5922-5934; DOI: 10.1523/JNEUROSCI.0330-19.2019

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Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex
Sze Chai Kwok (郭思齊), Yudian Cai (蔡禹甸), Mark J. Buckley
Journal of Neuroscience 24 July 2019, 39 (30) 5922-5934; DOI: 10.1523/JNEUROSCI.0330-19.2019
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Keywords

  • introspection
  • lesion
  • macaques
  • metacognition
  • prefrontal cortex
  • recognition memory

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