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

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.

Diffusion property and functional connectivity of superior longitudinal fasciculus underpin human metacognition

“…Additionally, it also lies within the frontal lobe, which is not mixed by the temporal fibres in the Arcuate Fasciculus (Wakana, 2007) and is indicative of the DLPFC -IPL communication (Yeatman et al, 2012). On one end, the right DLPFC is involved in both perceptual and mnemonic metacognition in both humans and monkeys, and suggested as reading out information related to primary decision-making and computing metacognitive judgements (Fleming and Dolan, 2012;Kwok et al, 2019;Morales et al, 2018;Shekhar and Rahnev, 2018).…”

“…As cognitive processes are implemented in the brain, an interesting and important question is whether the neural circuit supporting metacognition is the same or distinct across different cognitive domains.A large body of fMRI work have increasingly demonstrated a nuanced picture for this domaingenerality issue of metacognition. For example, the dorsolateral prefrontal cortex (DLPFC) might be involved in reading out the information of primary decision-making and using it for computing both perceptual and mnemonic metacognitive judgements (Chua and Ahmed, 2016;Fleming and Dolan, 2012;Kwok et al, 2019;Rounis et al, 2010). Morales et al (2018) reported that the dorsal anterior cingulate cortex (dACC) was active during metacognitive evaluation in both memory and perception tasks but also found the activation patterns decoded from a perception task in the posterior medial frontal cortex and ventral medial prefrontal cortex could predict metacognitive judgements in a memory task.…”

Total recall: episodic memory retrieval, choice, and memory confidence in the rat

“…We hypothesize that perceptual and memory confidence are integrated in decision-making, which optimally depends on evidence from varied sources, on long timescales. Prior to this step, different forms of memory confidence may be computed differently, by different circuits 35 .…”

“…While there is evidence that humans 32 and primates 12,[33][34][35] compute memory confidence, studies have focused exclusively on visual recognition memory [33][34][35][36] , which can be solved by familiarity rather than true episode recollection 37 . Thus, whether these findings generalize to episodic memories is unclear.…”

Use of Magnetic Resonance Spectroscopy to Explore Metacognitive Ability and Academic Score

“…Lesions to anterior prefrontal cortex impair perceptual metacognitive accuracy while sparing memory metacognitive accuracy [7][8]. Macaque monkey's metacognitive capability of introspecting its own memory success is causally dependent on intact superior dorsolateral prefrontal cortices but not the orbitofrontal cortices [9]. Studies in the past have indicated that variation in memory metacognitive efficiency was correlated with the volume of the precuneus [10].…”