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”) by two variants of meta-d'/d′ 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. Our 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.
Footnotes
The authors declare no competing financial interests.
This work is supported by the Ministry of Education of PRC Humanities and Social Sciences Research grant 16YJC190006, STCSM Natural Science Foundation of Shanghai 16ZR1410200, Fundamental Research Funds for the Central Universities 2018ECNU-HWFW007, NYU Shanghai and NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai (S.C.K.); and the U.K. Medical Research Council project grants G0300817 and MR/K005480/1 (M.J.B.). We thank Drs. Farshad Mansouri and Keiji Tanaka for allowing us to analyze the data that they obtained in some animals at the RIKEN Brain Science Institute.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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