Robotically-induced auditory-verbal hallucinations: combining self-monitoring and strong perceptual priors.

BACKGROUND: Inducing hallucinations under controlled experimental conditions in non-hallucinating individuals represents a novel research avenue oriented toward understanding complex hallucinatory phenomena, avoiding confounds observed in patients. Auditory-verbal hallucinations (AVH) are one of the most common and distressing psychotic symptoms, whose etiology remains largely unknown. Two prominent accounts portray AVH either as a deficit in auditory-verbal self-monitoring, or as a result of overly strong perceptual priors. METHODS: In order to test both theoretical models and evaluate their potential integration, we developed a robotic procedure able to induce self-monitoring perturbations (consisting of sensorimotor conflicts between poking movements and corresponding tactile feedback) and a perceptual prior associated with otherness sensations (i.e. feeling the presence of a non-existing another person). RESULTS: Here, in two independent studies, we show that this robotic procedure led to AVH-like phenomena in healthy individuals, quantified as an increase in false alarm rate in a voice detection task. Robotically-induced AVH-like sensations were further associated with delusional ideation and to both AVH accounts. Specifically, a condition with stronger sensorimotor conflicts induced more AVH-like sensations (self-monitoring), while, in the otherness-related experimental condition, there were more AVH-like sensations when participants were detecting other-voice stimuli, compared to detecting self-voice stimuli (strong-priors). CONCLUSIONS: By demonstrating an experimental procedure able to induce AVH-like sensations in non-hallucinating individuals, we shed new light on AVH phenomenology, thereby integrating self-monitoring and strong-priors accounts.

Confidence in visual detection, familiarity and recollection judgments is preserved in schizophrenia spectrum disorder.

An effective way to quantify metacognitive performance is to ask participants to estimate their confidence in the accuracy of their response during a cognitive task. A recent meta-analysis1 raised the issue that most assessments of metacognitive performance in schizophrenia spectrum disorders may be confounded with cognitive deficits, which are known to be present in this population. Therefore, it remains unclear whether the reported metacognitive deficits are metacognitive in nature or rather inherited from cognitive deficits. Arbitrating between these two possibilities requires equating task performance between experimental groups. Here, we aimed to characterize metacognitive performance among individuals with schizophrenia across three tasks (visual detection, familiarity, recollection) using a within-subject design while controlling experimentally for intra-individual task performance and statistically for between-subject task performance. In line with our hypotheses, we found no metacognitive deficit for visual detection and familiarity judgments. While we expected metacognition for recollection to be specifically impaired among individuals with schizophrenia, we found evidence in favor of an absence of a deficit in that domain also. We found no specific metacognitive deficit in schizophrenia spectrum disorder in the visual or memory domain. The clinical relevance of our findings is discussed in light of a hierarchical framework of metacognition.

Prior information differentially affects discrimination decisions and subjective confidence reports.

According to Bayesian models, both decisions and confidence are based on the same precision-weighted integration of prior expectations ("priors") and incoming information ("likelihoods"). This assumes that priors are integrated optimally and equally in decisions and confidence, which has not been tested. In three experiments, we quantify how priors inform decisions and confidence. With a dual-decision task we create pairs of conditions that are matched in posterior information, but differ on whether the prior or likelihood is more informative. We find that priors are underweighted in discrimination decisions, but are less underweighted in confidence about those decisions, and this is not due to differences in processing time. The same patterns remain with exogenous probabilistic cues as priors. With a Bayesian model we quantify the weighting parameters for the prior at both levels, and find converging evidence that priors are more optimally used in explicit confidence, even when underused in decisions.

Preserved electrophysiological markers of confidence in schizophrenia spectrum disorder.

A large number of behavioral studies suggest that confidence judgments are impaired in schizophrenia, motivating the search for neural correlates of an underlying metacognitive impairment. Electrophysiological studies suggest that a specific evoked response potential reflecting performance monitoring, namely the error-related negativity (ERN), is blunted in schizophrenia compared to healthy controls. However, attention has recently been drawn to a potential confound in the study of metacognition, namely that lower task-performance in schizophrenia compared to healthy controls involves a decreased index of metacognitive performance (where metacognitive performance is construed as the ability to calibrate one's confidence relative to response correctness), independently of metacognitive abilities among patients. Here, we assessed how this confound might also apply to ERN-blunting in schizophrenia. We used an adaptive staircase procedure to titrate task-performance on a motion discrimination task in which participants (N = 14 patients and 19 controls) had to report their confidence after each trial while we recorded high density EEG. Interestingly, not only metaperceptual abilities were preserved among patients at the behavioral level, but contrary to our hypothesis, we also found no electrophysiological evidence for altered EEG markers of performance monitoring. These results bring additional evidence suggesting an unaltered ability to monitor perceptual performance on a trial by trial basis in schizophrenia.

Bone conduction facilitates self-other voice discrimination.

One's own voice is one of the most important and most frequently heard voices. Although it is the sound we associate most with ourselves, it is perceived as strange when played back in a recording. One of the main reasons is the lack of bone conduction that is inevitably present when hearing one's own voice while speaking. The resulting discrepancy between experimental and natural self-voice stimuli has significantly impeded self-voice research, rendering it one of the least investigated aspects of self-consciousness. Accordingly, factors that contribute to self-voice perception remain largely unknown. In a series of three studies, we rectified this ecological discrepancy by augmenting experimental self-voice stimuli with bone-conducted vibrotactile stimulation that is present during natural self-voice perception. Combining voice morphing with psychophysics, we demonstrate that specifically self-other but not familiar-other voice discrimination improved for stimuli presented using bone as compared with air conduction. Furthermore, our data outline independent contributions of familiarity and acoustic processing to separating the own from another's voice: although vocal differences increased general voice discrimination, self-voices were more confused with familiar than unfamiliar voices, regardless of their acoustic similarity. Collectively, our findings show that concomitant vibrotactile stimulation improves auditory self-identification, thereby portraying self-voice as a fundamentally multi-modal construct.

Relationships between neuropsychological performance, insight, medication adherence, and social metacognition in schizophrenia.

BACKGROUND: Social metacognition is still poorly understood in schizophrenia, particularly its neuropsychological basis and its impact on insight and medication adherence. We therefore quantified social metacognition as the agreement between objective and subjective mentalization and assessed its correlates in a sample of individuals with schizophrenia spectrum disorders. METHODS: Participants consisted of 143 patients with schizophrenia or schizoaffective disorders who underwent a metacognitive version of a mentalization task, an extensive neuropsychological battery, and a clinical evaluation to assess their insight into illness and medication adherence. We studied potential interactions between confidence judgments and several neuropsychological and clinical variables on mentalization accuracy with mixed-effects multiple logistic regressions. RESULTS: Confidence judgments were closely associated with mentalization accuracy, indicative of good social metacognition in this task. Working memory, visual memory, and reasoning and problem-solving were the three neuropsychological dimensions positively associated with metacognition. By contrast, the two measures of medication adherence were associated with poorer metacognition, whereas no association was found between metacognition and clinical insight. The multiple regression model showed a significant positive impact of better working memory, older age at onset, longer duration of hospitalization, and worse medication adherence on social metacognition. CONCLUSIONS: We discuss possible mechanisms underlying the apparent association between social metacognition and working memory. Adherence should be monitored when remediating social metacognition, and psychoeducation should be given to patients with a high level of awareness of their capacity to mentalize.

The Scientific Study of Consciousness Cannot and Should Not Be Morally Neutral.

A target question for the scientific study of consciousness is how dimensions of consciousness, such as the ability to feel pain and pleasure or reflect on one's own experience, vary in different states and animal species. Considering the tight link between consciousness and moral status, answers to these questions have implications for law and ethics. Here we point out that given this link, the scientific community studying consciousness may face implicit pressure to carry out certain research programs or interpret results in ways that justify current norms rather than challenge them. We show that because consciousness largely determines moral status, the use of nonhuman animals in the scientific study of consciousness introduces a direct conflict between scientific relevance and ethics-the more scientifically valuable an animal model is for studying consciousness, the more difficult it becomes to ethically justify compromises to its well-being for consciousness research. Finally, in light of these considerations, we call for a discussion of the immediate ethical corollaries of the body of knowledge that has accumulated and for a more explicit consideration of the role of ideology and ethics in the scientific study of consciousness.

Consensus Goals in the Field of Visual Metacognition.

Despite the tangible progress in psychological and cognitive sciences over the last several years, these disciplines still trail other more mature sciences in identifying the most important questions that need to be solved. Reaching such consensus could lead to greater synergy across different laboratories, faster progress, and increased focus on solving important problems rather than pursuing isolated, niche efforts. Here, 26 researchers from the field of visual metacognition reached consensus on four long-term and two medium-term common goals. We describe the process that we followed, the goals themselves, and our plans for accomplishing these goals. If this effort proves successful within the next few years, such consensus building around common goals could be adopted more widely in psychological science.

Impaired sense of agency and associated confidence in psychosis.

The Sense of Agency (SoA), our sensation of control over our actions, is a fundamental mechanism for delineating the Self from the environment and others. SoA arises from implicit processing of sensorimotor signals as well as explicit higher-level judgments. Psychosis patients suffer from difficulties in the sense of control over their actions and accurate demarcation of the Self. Moreover, it is unclear if they have metacognitive insight into their aberrant abilities. In this pre-registered study, we examined SoA and its associated confidence judgments using an embodied virtual reality paradigm in psychosis patients and controls. Our results show that psychosis patients not only have a severely reduced ability for discriminating their actions but they also do not show proper metacognitive insight into this deficit. Furthermore, an exploratory analysis revealed that the SoA capacities allow for high levels of accuracy in clinical classification of psychosis. These results indicate that SoA and its metacognition are core aspects of the psychotic state and provide possible venues for understanding the underlying mechanisms of psychosis, that may be leveraged for novel clinical purposes.

Sense of self impacts spatial navigation and hexadirectional coding in human entorhinal cortex.

Grid cells in entorhinal cortex (EC) encode an individual's location in space and rely on environmental cues and self-motion cues derived from the individual's body. Body-derived signals are also primary signals for the sense of self and based on integrated sensorimotor signals (proprioceptive, tactile, visual, motor) that have been shown to enhance self-centered processing. However, it is currently unknown whether such sensorimotor signals that modulate self-centered processing impact grid cells and spatial navigation. Integrating the online manipulation of bodily signals, to modulate self-centered processing, with a spatial navigation task and an fMRI measure to detect grid cell-like representation (GCLR) in humans, we report improved performance in spatial navigation and decreased GCLR in EC. This decrease in entorhinal GCLR was associated with an increase in retrosplenial cortex activity, which was correlated with participants' navigation performance. These data link self-centered processes during spatial navigation to entorhinal and retrosplenial activity and highlight the role of different bodily factors at play when navigating in VR.

A leaky evidence accumulation process for perceptual experience.

The neural correlates supporting our perceptual experience of the world remain largely unknown. Recent studies have shown how stimulus detection and related confidence involve evidence accumulation (EA) processes similar to those involved in perceptual decision-making. Here, we propose that independently from any tasks, percepts are not static but fade in and out of consciousness according to the dynamics of a leaky evidence accumulation process (LEAP), and that confidence corresponds to the maximal evidence accumulated by this process. We discuss the implications and limitations of our proposal, assess how it may qualify as a neural correlate of consciousness, and illustrate how it brings us closer to a mechanistic understanding of phenomenal aspects of perceptual experience like intensity and duration, beyond mere detection.

No evidence of impaired visual and tactile metacognition in adults with tourette disorder.

INTRODUCTION: Premonitory urges in Tourette disorder are often linked to altered somatosensory processing, which might include deficits in metacognition. We explored tactile and visual metacognitive ability in people with Tourette disorder and healthy control participants. METHODS: Patients with Tourrete disorder and healthy control participants completed a tactile and a visual metacognitive task. On each trial, participants did a forced choice discrimination and then rated their confidence in their decision. To quantify metacognitive ability, we used m-ratio - a bias-free measure that allows for comparisons across modalities. Correlations between severity of tics and premonitory urges with tactile metacognitive sensitivity were also performed. RESULTS: Metacognitive ability in both tactile and visual domains was comparable between adults with Tourette disorder and healthy controls. We also found no evidence for correlations between tactile metacognitive ability and severity of premonitory urges or tic severity. CONCLUSIONS: Tactile and visual metacognition is not impaired in adults with Tourette disorder. These results question the role of altered tactile metacognition in pathophysiology of tic disorders.

Breathing affects self-other voice discrimination in a bodily state associated with somatic passivity.

A growing number of studies have focused on identifying cognitive processes that are modulated by interoceptive signals, particularly in relation to the respiratory or cardiac cycle. Considering the fundamental role of interoception in bodily self-consciousness, we here investigated whether interoceptive signals also impact self-voice perception. We applied an interactive, robotic paradigm associated with somatic passivity (a bodily state characterized by illusory misattribution of self-generated touches to someone else) to investigate whether somatic passivity impacts self-voice perception as a function of concurrent interoceptive signals. Participants' breathing and heartbeat signals were recorded while they performed two self-voice tasks (self-other voice discrimination and loudness perception) and while simultaneously experiencing two robotic conditions (somatic passivity condition; control condition). Our data reveal that respiration, but not cardiac activity, affects self-voice perception: participants were better at discriminating self-voice from another person's voice during the inspiration phase of the respiration cycle. Moreover, breathing effects were prominent in participants experiencing somatic passivity and a different task with the same stimuli (i.e., judging the loudness and not identity of the voices) was unaffected by breathing. Combining interoception and voice perception with self-monitoring framework, these data extend findings on breathing-dependent changes in perception and cognition to self-related processing.

Metacognitive improvement: Disentangling adaptive training from experimental confounds.

Metacognition is defined as the capacity to monitor and control one's own cognitive processes. Recently, Carpenter and colleagues (2019) reported that metacognitive performance can be improved through adaptive training: healthy participants performed a perceptual discrimination task, and subsequently indicated confidence in their response. Metacognitive performance, defined as how much information these confidence judgments contain about the accuracy of perceptual decisions, was found to increase in a group of participants receiving monetary reward based on their confidence judgments over hundreds of trials and multiple sessions. By contrast, in a control group where only perceptual performance was incentivized, metacognitive performance remained constant across experimental sessions. We identified two possible confounds that may have led to an artificial increase in metacognitive performance, namely the absence of reward in the initial session and an inconsistency between the reward scheme and the instructions about the confidence scale. We thus conducted a preregistered conceptual replication where all sessions were rewarded and where instructions were consistent with the reward scheme. Critically, once these two confounds were corrected we found moderate evidence for an absence of metacognitive training. Our data thus suggest that previous claims about metacognitive training are premature, and calls for more research on how to train individuals to monitor their own performance. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Sense of agency for intracortical brain-machine interfaces.

Intracortical brain-machine interfaces decode motor commands from neural signals and translate them into actions, enabling movement for paralysed individuals. The subjective sense of agency associated with actions generated via intracortical brain-machine interfaces, the neural mechanisms involved and its clinical relevance are currently unknown. By experimentally manipulating the coherence between decoded motor commands and sensory feedback in a tetraplegic individual using a brain-machine interface, we provide evidence that primary motor cortex processes sensory feedback, sensorimotor conflicts and subjective states of actions generated via the brain-machine interface. Neural signals processing the sense of agency affected the proficiency of the brain-machine interface, underlining the clinical potential of the present approach. These findings show that primary motor cortex encodes information related to action and sensing, but also sensorimotor and subjective agency signals, which in turn are relevant for clinical applications of brain-machine interfaces.

Robotically-induced hallucination triggers subtle changes in brain network transitions.

The perception that someone is nearby, although nobody can be seen or heard, is called presence hallucination (PH). Being a frequent hallucination in patients with Parkinson's disease, it has been argued to be indicative of a more severe and rapidly advancing form of the disease, associated with psychosis and cognitive decline. PH may also occur in healthy individuals and has recently been experimentally induced, in a controlled manner during fMRI, using MR-compatible robotics and sensorimotor stimulation. Previous neuroimaging correlates of such robot-induced PH, based on conventional time-averaged fMRI analysis, identified altered activity in the posterior superior temporal sulcus and inferior frontal gyrus in healthy individuals. However, no link with the strength of the robot-induced PH was observed, and such activations were also associated with other sensations induced by robotic stimulation. Here we leverage recent advances in dynamic functional connectivity, which have been applied to different psychiatric conditions, to decompose fMRI data during PH-induction into a set of co-activation patterns that are tracked over time, as to characterize their occupancies, durations, and transitions. Our results reveal that, when PH is induced, the identified brain patterns significantly and selectively increase their transition probabilities towards a specific brain pattern, centred on the posterior superior temporal sulcus, angular gyrus, dorso-lateral prefrontal cortex, and middle prefrontal cortex. This change is not observed in any other control conditions, nor is it observed in association with other sensations induced by robotic stimulation. The present findings describe the neural mechanisms of PH in healthy individuals and identify a specific disruption of the dynamics of network interactions, extending previously reported network dysfunctions in psychotic patients with hallucinations to an induced robot-controlled specific hallucination in healthy individuals.

Agency Deficits in a Human Genetic Model of Schizophrenia: Insights From 22q11DS Patients.

Schizophrenia is a chronic and disabling mental illness characterized by a disordered sense of self. Current theories suggest that deficiencies in the sense of control over one's actions (Sense of Agency, SoA) may underlie some of the symptoms of schizophrenia. However, it is not clear if agency deficits are a precursor or a result of psychosis. Here, we investigated full body agency using virtual reality in a cohort of 22q11 deletion syndrome participants with a genetic propensity for schizophrenia. In two experiments employing virtual reality, full body motion tracking, and online feedback, we investigated SoA in two separate domains. Our results show that participants with 22q11DS had a considerable deficit in monitoring their actions, compared to age-matched controls in both the temporal and spatial domain. This was coupled with a bias toward erroneous attribution of actions to the self. These results indicate that nonpsychotic 22q11DS participants have a domain general deficit in the conscious sensorimotor mechanisms underlying the bodily self. Our data reveal an abnormality in the SoA in a cohort with a genetic predisposition for schizophrenia, but without psychosis, providing evidence that deficits in delineation of the self may be a precursor rather than a result of the psychotic state.

Exploring Clinical Correlates of Metacognition in Bipolar Disorders Using Moderation Analyses: The Role of Antipsychotics.

The determinants of metacognition are still poorly understood in bipolar disorders (BD). We aimed to examine the clinical determinants of metacognition, defined as the agreement between objective and subjective cognition in individuals with BD. The participants consisted of 281 patients with BD who underwent an extensive neuropsychological battery and clinical evaluation. To assess subjective cognition, participants provided a general rating of their estimated cognitive difficulties. Clinical characteristics of BD were also recorded, along with medication. We studied the potential moderation of the association between cognitive complaints and global objective cognitive performance by several clinical variables with ordinal logistic regressions. Depression and impulsivity were associated with greater cognitive complaints. The only variable that moderated the relationship between objective and subjective cognition in the global model was the prescription of antipsychotics. Patients taking antipsychotics had a poorer association between cognitive complaints and objective neuropsychological performance. This result suggests a role for dopamine in the modulation of metacognitive performance, and calls for the systematic control of antipsychotic medication in future studies documenting metacognitive deficits in severe and persistent mental disorders. Depression and impulsivity should be investigated as potential therapeutic targets for individuals with BD and cognitive complaints, before proposing an extensive neuropsychological evaluation.

Increased Functional Connectivity of the Intraparietal Sulcus Underlies the Attenuation of Numerosity Estimations for Self-Generated Words.

Previous studies have shown that self-generated stimuli in auditory, visual, and somatosensory domains are attenuated, producing decreased behavioral and neural responses compared with the same stimuli that are externally generated. Yet, whether such attenuation also occurs for higher-level cognitive functions beyond sensorimotor processing remains unknown. In this study, we assessed whether cognitive functions such as numerosity estimations are subject to attenuation in 56 healthy participants (32 women). We designed a task allowing the controlled comparison of numerosity estimations for self-generated (active condition) and externally generated (passive condition) words. Our behavioral results showed a larger underestimation of self-generated compared with externally generated words, suggesting that numerosity estimations for self-generated words are attenuated. Moreover, the linear relationship between the reported and actual number of words was stronger for self-generated words, although the ability to track errors about numerosity estimations was similar across conditions. Neuroimaging results revealed that numerosity underestimation involved increased functional connectivity between the right intraparietal sulcus and an extended network (bilateral supplementary motor area, left inferior parietal lobule, and left superior temporal gyrus) when estimating the number of self-generated versus externally generated words. We interpret our results in light of two models of attenuation and discuss their perceptual versus cognitive origins.SIGNIFICANCE STATEMENT We perceive sensory events as less intense when they are self-generated compared with when they are externally generated. This phenomenon, called attenuation, enables us to distinguish sensory events from self and external origins. Here, we designed a novel fMRI paradigm to assess whether cognitive processes such as numerosity estimations are also subject to attenuation. When asking participants to estimate the number of words they had generated or passively heard, we found bigger underestimation in the former case, providing behavioral evidence of attenuation. Attenuation was associated with increased functional connectivity of the intraparietal sulcus, a region involved in numerosity processing. Together, our results indicate that the attenuation of self-generated stimuli is not limited to sensory consequences but is also impact cognitive processes such as numerosity estimations.

Evidence accumulation relates to perceptual consciousness and monitoring.

A fundamental scientific question concerns the neural basis of perceptual consciousness and perceptual monitoring resulting from the processing of sensory events. Although recent studies identified neurons reflecting stimulus visibility, their functional role remains unknown. Here, we show that perceptual consciousness and monitoring involve evidence accumulation. We recorded single-neuron activity in a participant with a microelectrode in the posterior parietal cortex, while they detected vibrotactile stimuli around detection threshold and provided confidence estimates. We find that detected stimuli elicited neuronal responses resembling evidence accumulation during decision-making, irrespective of motor confounds or task demands. We generalize these findings in healthy volunteers using electroencephalography. Behavioral and neural responses are reproduced with a computational model considering a stimulus as detected if accumulated evidence reaches a bound, and confidence as the distance between maximal evidence and that bound. We conclude that gradual changes in neuronal dynamics during evidence accumulation relates to perceptual consciousness and perceptual monitoring in humans.