Individual susceptibility to TMS affirms the precuneal role in meta-memory upon recollection

Ye, Qun; Zou, Futing; Dayan, Michael; Lau, Hakwan; Hu, Yi; Kwok, Sze Chai

doi:10.1007/s00429-019-01909-6

Cited by 44 publications

(41 citation statements)

References 54 publications

(64 reference statements)

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“…Intrinsic individual differences in functional connectivity between brain structures have informed our understanding of the varied ability to introspect about self-performance (Baird et al, 2013; Fleming et al, 2010; Ye et al, 2019). Here we found that resting-state functional connectivity of hippocampus and angular gyrus is specifically associated with vividness efficiency, while the connectivity of hippocampus and medial aPFC predicts metacognitive efficiency across individuals.…”

Section: Discussionmentioning

confidence: 99%

Distinct generation of subjective vividness and confidence during naturalistic memory retrieval in angular gyrus

Zou

Kwok

2021

Preprint

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Subjective experience of remembering is a hallmark of episodic memory, which enables us to monitor experiences, identify mistakes, and adjust our decisions accordingly. A fundamental and enduring puzzle is the origin of confidence in memory; for example, does the confidence during episodic retrieval depend upon the subjective sensed vividness, or does confidence and vividness reflect dissociable introspective processes? The angular gyrus (AnG) exhibits a sensitivity to subjective experience of remembering, but its direct contribution to the monitoring of internal subjective mnemonic experience has hitherto been lacking. Here we combined a novel naturalistic video-watching paradigm with repetitive transcranial magnetic stimulation (rTMS) and resting-state functional magnetic resonance imaging (fMRI) to test the idea that vividness and confidence are generated differently during retrieval. We found that pre-retrieval rTMS targeting the left AnG selectively alters the vividness efficiency compared to control stimulation while keeping metacognitive efficiency and objective memory accuracy unaffected. Using trial-wise data, we showed that vividness mediates the association between confidence and objective memory accuracy and such mediation was eradicated by AnG stimulation. Furthermore, resting-state functional connectivity of hippocampus and AnG was specifically associated with vividness efficiency, while the connectivity of hippocampus and medial prefrontal cortex was associated with metacognitive efficiency across individuals. These findings identify a role for the AnG in gauging the vividness, but not the confidence, of memory, thereby providing evidence for a differentiation account of conscious assessment of memory by functionally and anatomically dissociating the monitoring of vividness from confidence.

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Section: Discussionmentioning

confidence: 99%

Distinct generation of subjective vividness and confidence during naturalistic memory retrieval in angular gyrus

Zou

Kwok

2021

Preprint

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“…This suggests that the IPL -DLPFC network makes use of the memory information from the precuneus for metacognitive decisions. Together with the precuneus -hippocampus connectivity (Ye et al, 2019), a cortico-hippocampal network of meta-mnemonic process is at work with primary mnemonic processes (McClelland et al, 1995;Wang et al, 2014;Zeidman et al, 2015), implicating the hippocampus in initiating the retrieval of the memory traces, which are then integrated to detailed recollections and conscious monitoring supported by the precuneus and the IPL (Richter et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

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

Zheng

Wang

et al. 2020

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Metacognition as the capacity of monitoring one's own cognition operates across domains.Here, we addressed whether metacognition in different cognitive domains rely on common or distinct neural substrates with diffusion tensor imaging (DTI) and inter-areal functional connectivity techniques. After acquiring DTI and resting-state fMRI data, we asked participants to perform a temporal-order memory judgement task and a perceptual discrimination task, followed by trial-specific confidence judgments. DTI analysis revealed that the structural integrity (fractional anisotropy) in the anterior portion of right superior longitudinal fasciculus (SLF) was associated with both perceptual and mnemonic metacognitive abilities. When the mnemonic metacognitive ability was disrupted by TMS, the mnemonic metacognition scores did not correlate with SLF structural integrity anymore, revealing the causal relevance of this tract in memory metacognition. Furthermore, taking the dorsolateral PFC and IPL (both of which are connected by SLF) as seeds, we found perceptual and mnemonic metacognitive abilities to be associated with functional connectivity between DLPFC and VLPFC, whereas mnemonic metacognitive ability was selectively associated with connectivity between IPL and precuneus. These results illustrate the importance of SLF and a distinct white-matter grey-matter circuitry that supports human metacognition. Introduction:The capacity of reflecting on one's own cognitive process is known as metacognition (Flavell, 1979;Fleming and Dolan, 2012;Yeung and Summerfield, 2012). Metacognition has been considered as the most crucial function emerged during evolution (Hayes, 2016). Given its crucial functions, researchers have endeavored to understand how a metacognitive judgment is computed (Fleming and Daw, 2017;Kepecs et al., 2008;Zylberberg et al., 2016), how it is disrupted in psychiatric disorders (Hauser et al., 2017a;Rouault et al., 2018a), and how its accuracy can be improved (Carpenter et al., 2019). Metacognition is an umbrella term for the higher-level cognition about the lower-level cognition in various domains (e.g., perception and memory). 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 ven...

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“…Indeed, previous studies tapping into the OFC role in meta-related processes were all on perceptual decisions, such as odor discrimination judgment (Kepecs et al, 2008; Lak et al, 2014), whereas at present the tasks in question concern mnemonic decisions. Some recent work on humans has similarly evinced such specificity for perceptual versus memory related metacognition (Fleming et al, 2014; Ye et al, 2018, 2019).…”

Section: Discussionmentioning

confidence: 99%

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

2019

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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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Individual susceptibility to TMS affirms the precuneal role in meta-memory upon recollection

Cited by 44 publications

References 54 publications

Distinct generation of subjective vividness and confidence during naturalistic memory retrieval in angular gyrus

Distinct generation of subjective vividness and confidence during naturalistic memory retrieval in angular gyrus

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

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

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