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.

Disentangling the origins of confidence in speeded perceptual judgments through multimodal imaging.

The human capacity to compute the likelihood that a decision is correct-known as metacognition-has proven difficult to study in isolation as it usually cooccurs with decision making. Here, we isolated postdecisional from decisional contributions to metacognition by analyzing neural correlates of confidence with multimodal imaging. Healthy volunteers reported their confidence in the accuracy of decisions they made or decisions they observed. We found better metacognitive performance for committed vs. observed decisions, indicating that committing to a decision may improve confidence. Relying on concurrent electroencephalography and hemodynamic recordings, we found a common correlate of confidence following committed and observed decisions in the inferior frontal gyrus and a dissociation in the anterior prefrontal cortex and anterior insula. We discuss these results in light of decisional and postdecisional accounts of confidence and propose a computational model of confidence in which metacognitive performance naturally improves when evidence accumulation is constrained upon committing a decision.

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.

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.

Confidence in visual motion discrimination is preserved in individuals with schizophrenia.

BACKGROUND: Metacognition is the set of reflexive processes that allows humans to evaluate the accuracy of their mental operations. Metacognitive deficits have been described in people with schizophrenia using mostly narrative assessment, and they have been linked to several key symptoms. METHODS: We assessed metacognitive performance objectively by asking people with schizophrenia or schizoaffective disorder (n = 20) and matched healthy participants (n = 21) to perform a visual discrimination task and report their confidence in their performance. Metacognitive performance was defined as the adequacy between visual discrimination performance and confidence. RESULTS: Bayesian analyses revealed equivalent metacognitive performance in the 2 groups, despite a weaker association between confidence and trajectory tracking during task execution among people with schizophrenia. We reproduced these results using an evidence accumulation model, which showed similar decisional processes in the 2 groups. LIMITATIONS: These results from a relatively small study sample cannot be generalized to other perceptual and nonperceptual tasks. To meet this purpose, ecological tasks are needed. As well, the role of antipsychotic medication and design deserves greater attention in the future. CONCLUSION: We found similar decisional and metacognitive capabilities between people with schizophrenia and healthy controls in a visual discrimination task.

First-person body view modulates the neural substrates of episodic memory and autonoetic consciousness: A functional connectivity study.

Episodic memory (EM) is classically conceived as a memory for events, localized in space and time, and characterized by autonoetic consciousness (ANC) allowing to mentally travel back in time and subjectively relive an event. Building on recent evidence that the first-person visual co-perception of one's own body during encoding impacts EM, we used a scene recognition task in immersive virtual reality (VR) and measured how first-person body view would modulate peri-encoding resting-state fMRI, EM performance, and ANC. Specifically, we investigated the impact of body view on post-encoding functional connectivity in an a priori network of regions related either to EM or multisensory bodily processing and used these regions in a seed-to-whole brain analysis. Post-encoding connectivity between right hippocampus (rHC) and right parahippocampus (rPHC) was enhanced when participants encoded scenes while seeing their body. Moreover, the strength of connectivity between the rHC, rPHC and the neocortex displayed two main patterns with respect to body view. The connectivity with a sensorimotor fronto-parietal network, comprising primary somatosensory and primary motor cortices, correlated with ANC after - but not before - encoding, depending on body view. The opposite change of connectivity was found between rHC, rPHC and the medial parietal cortex (from being correlated with ANC before encoding to an absence of correlation after encoding), but irrespective of body view. Linking immersive VR and fMRI for the study of EM and ANC, these findings suggest that seeing one's own body during encoding impacts the brain activity related to EM formation by modulating the connectivity between the right hippocampal formation and the neocortical regions involved in the processing of multisensory bodily signals and self-consciousness.

Behavioral, Modeling, and Electrophysiological Evidence for Supramodality in Human Metacognition.

Human metacognition, or the capacity to introspect on one's own mental states, has been mostly characterized through confidence reports in visual tasks. A pressing question is to what extent results from visual studies generalize to other domains. Answering this question allows determining whether metacognition operates through shared, supramodal mechanisms or through idiosyncratic, modality-specific mechanisms. Here, we report three new lines of evidence for decisional and postdecisional mechanisms arguing for the supramodality of metacognition. First, metacognitive efficiency correlated among auditory, tactile, visual, and audiovisual tasks. Second, confidence in an audiovisual task was best modeled using supramodal formats based on integrated representations of auditory and visual signals. Third, confidence in correct responses involved similar electrophysiological markers for visual and audiovisual tasks that are associated with motor preparation preceding the perceptual judgment. We conclude that the supramodality of metacognition relies on supramodal confidence estimates and decisional signals that are shared across sensory modalities.SIGNIFICANCE STATEMENT Metacognitive monitoring is the capacity to access, report, and regulate one's own mental states. In perception, this allows rating our confidence in what we have seen, heard, or touched. Although metacognitive monitoring can operate on different cognitive domains, we ignore whether it involves a single supramodal mechanism common to multiple cognitive domains or modality-specific mechanisms idiosyncratic to each domain. Here, we bring evidence in favor of the supramodality hypothesis by showing that participants with high metacognitive performance in one modality are likely to perform well in other modalities. Based on computational modeling and electrophysiology, we propose that supramodality can be explained by the existence of supramodal confidence estimates and by the influence of decisional cues on confidence estimates.

Audio-Tactile and Peripersonal Space Processing Around the Trunk in Human Parietal and Temporal Cortex: An Intracranial EEG Study.

Interactions with the environment happen within one's peripersonal space (PPS)-the space surrounding the body. Studies in monkeys and humans have highlighted a multisensory distributed cortical network representing the PPS. However, knowledge about the temporal dynamics of PPS processing around the trunk is lacking. Here, we recorded intracranial electroencephalography (iEEG) in humans while administering tactile stimulation (T), approaching auditory stimuli (A), and the 2 combined (AT). To map PPS, tactile stimulation was delivered when the sound was far, intermediate, or close to the body. The 19% of the electrodes showed AT multisensory integration. Among those, 30% showed a PPS effect, a modulation of the response as a function of the distance between the sound and body. AT multisensory integration and PPS effects had similar spatiotemporal characteristics, with an early response (~50 ms) in the insular cortex, and later responses (~200 ms) in precentral and postcentral gyri. Superior temporal cortex showed a different response pattern with AT multisensory integration at ~100 ms without a PPS effect. These results, represent the first iEEG delineation of PPS processing in humans and show that PPS and multisensory integration happen at similar neural sites and time periods, suggesting that PPS representation is based on a spatial modulation of multisensory integration.

Self-Grounded Vision: Hand Ownership Modulates Visual Location through Cortical ß and γ Oscillations.

Vision is known to be shaped by context, defined by environmental and bodily signals. In the Taylor illusion, the size of an afterimage projected on one's hand changes according to proprioceptive signals conveying hand position. Here, we assessed whether the Taylor illusion does not just depend on the physical hand position, but also on bodily self-consciousness as quantified through illusory hand ownership. Relying on the somatic rubber hand illusion, we manipulated hand ownership, such that participants embodied a rubber hand placed next to their own hand. We found that an afterimage projected on the participant's hand drifted depending on illusory ownership between the participants' two hands, showing an implication of self-representation during the Taylor illusion. Oscillatory power analysis of electroencephalographic signals showed that illusory hand ownership was stronger in participants with stronger α suppression over left sensorimotor cortex, whereas the Taylor illusion correlated with higher ß/γ power over frontotemporal regions. Higher γ connectivity between left sensorimotor and inferior parietal cortex was also found during illusory hand ownership. These data show that afterimage drifts in the Taylor illusion do not only depend on the physical hand position but also on subjective ownership, which itself is based on the synchrony of somatosensory signals from the two hands. The effect of ownership on afterimage drifts is associated with ß/γ power and γ connectivity between frontoparietal regions and the visual cortex. Together, our results suggest that visual percepts are not only influenced by bodily context but are self-grounded, mapped on a self-referential frame. SIGNIFICANCE STATEMENT: Vision is influenced by the body: in the Taylor illusion, the size of an afterimage projected on one's hand changes according to tactile and proprioceptive signals conveying hand position. Here, we report a new phenomenon revealing that the perception of afterimages depends not only on bodily signals, but also on the sense of self. Relying on the rubber hand illusion, we manipulated hand ownership, so that participants embodied a rubber hand placed next to their own hand. We found that visual afterimages projected on the participant's hand drifted laterally, only when the rubber hand was embodied. Electroencephalography revealed spectral dissociations between somatic and visual effects, and higher γ connectivity along the dorsal visual pathways when the rubber hand was embodied.

The Insula Mediates Access to Awareness of Visual Stimuli Presented Synchronously to the Heartbeat.

UNLABELLED: The processing of interoceptive signals in the insular cortex is thought to underlie self-awareness. However, the influence of interoception on visual awareness and the role of the insular cortex in this process remain unclear. Here, we show in a series of experiments that the relative timing of visual stimuli with respect to the heartbeat modulates visual awareness. We used two masking techniques and show that conscious access for visual stimuli synchronous to participants' heartbeat is suppressed compared with the same stimuli presented asynchronously to their heartbeat. Two independent brain imaging experiments using high-resolution fMRI revealed that the insular cortex was sensitive to both visible and invisible cardio-visual stimulation, showing reduced activation for visual stimuli presented synchronously to the heartbeat. Our results show that interoceptive insular processing affects visual awareness, demonstrating the role of the insula in integrating interoceptive and exteroceptive signals and in the processing of conscious signals beyond self-awareness. SIGNIFICANCE STATEMENT: There is growing evidence that interoceptive signals conveying information regarding the internal state of the body influence perception and self-awareness. The insular cortex, which receives sensory inputs from both interoceptive and exteroceptive sources, is thought to integrate these multimodal signals. This study shows that cardiac interoceptive signals modulate awareness for visual stimuli such that visual stimuli occurring at the cardiac frequency take longer to access visual awareness and are more difficult to discriminate. Two fMRI experiments show that the insular region is sensitive to this cardio-visual synchrony even when the visual stimuli are rendered invisible through interocular masking. The results indicate a perceptual and neural suppression for visual events coinciding with cardiac interoceptive signals.

Low-level awareness accompanies "unconscious" high-level processing during continuous flash suppression.

The scope and limits of unconscious processing are a matter of ongoing debate. Lately, continuous flash suppression (CFS), a technique for suppressing visual stimuli, has been widely used to demonstrate surprisingly high-level processing of invisible stimuli. Yet, recent studies showed that CFS might actually allow low-level features of the stimulus to escape suppression and be consciously perceived. The influence of such low-level awareness on high-level processing might easily go unnoticed, as studies usually only probe the visibility of the feature of interest, and not that of lower-level features. For instance, face identity is held to be processed unconsciously since subjects who fail to judge the identity of suppressed faces still show identity priming effects. Here we challenge these results, showing that such high-level priming effects are indeed induced by faces whose identity is invisible, but critically, only when a lower-level feature, such as color or location, is visible. No evidence for identity processing was found when subjects had no conscious access to any feature of the suppressed face. These results suggest that high-level processing of an image might be enabled by-or co-occur with-conscious access to some of its low-level features, even when these features are not relevant to the processed dimension. Accordingly, they call for further investigation of lower-level awareness during CFS, and reevaluation of other unconscious high-level processing findings.

Enhanced discriminability for nonbiological motion violating the two-thirds power law.

The two-thirds power law describes the relationship between velocity and curvature in human motor movements. Interestingly, this motor law also affects visual motion perception, in which stimuli moving according to the two-thirds power law are perceived to have a constant velocity compared to stimuli actually moving at constant velocity. Thus, visual motion adhering to biological motion principles causes a kinematic illusion of smooth and velocity-invariant motion. However, it is yet unclear how this motion law affects the discrimination of visual stimuli and if its encoding requires attention. Here we tested the perceptual discrimination of stimuli following biological (two-thirds power law) or nonbiological movement under conditions in which the stimuli were degraded or masked through continuous flash suppression. Additionally, we tested subjective perception of naturalness and velocity consistency. Our results show that the discriminability of a visual target is inversely related to the perceived "naturalness" of its movement. Discrimination of stimuli following the two-thirds power law required more time than the same stimuli moving at constant velocity or nonecological variants of the two-thirds power law and was present for both masked and degraded stimuli.

Visual consciousness and bodily self-consciousness.

PURPOSE OF REVIEW: In recent years, consciousness has become a central topic in cognitive neuroscience. This review focuses on the relation between bodily self-consciousness - the feeling of being a subject in a body - and visual consciousness - the subjective experience associated with the perception of visual signals. RECENT FINDINGS: Findings from clinical and experimental work have shown that bodily self-consciousness depends on specific brain networks and is related to the integration of signals from multiple sensory modalities including vision. In addition, recent experiments have shown that visual consciousness is shaped by the body, including vestibular, tactile, proprioceptive, and motor signals. SUMMARY: Several lines of evidence suggest reciprocal relationships between vision and bodily signals, indicating that a comprehensive understanding of visual and bodily self-consciousness requires studying them in unison.

Multisensory integration in complete unawareness: evidence from audiovisual congruency priming.

Multisensory integration is thought to require conscious perception. Although previous studies have shown that an invisible stimulus could be integrated with an audible one, none have demonstrated integration of two subliminal stimuli of different modalities. Here, pairs of identical or different audiovisual target letters (the sound /b/ with the written letter "b" or "m," respectively) were preceded by pairs of masked identical or different audiovisual prime digits (the sound /6/ with the written digit "6" or "8," respectively). In three experiments, awareness of the audiovisual digit primes was manipulated, such that participants were either unaware of the visual digit, the auditory digit, or both. Priming of the semantic relations between the auditory and visual digits was found in all experiments. Moreover, a further experiment showed that unconscious multisensory integration was not obtained when participants did not undergo prior conscious training of the task. This suggests that following conscious learning, unconscious processing suffices for multisensory integration.

Nonconscious learning from crowded sequences.

Can people learn complex information without conscious awareness? Implicit learning-learning without awareness of what has been learned-has been the focus of intense investigation over the last 50 years. However, it remains controversial whether complex knowledge can be learned implicitly. In the research reported here, we addressed this challenge by asking participants to differentiate between sequences of symbols they could not perceive consciously. Using an operant-conditioning task, we showed that participants learned to associate distinct sequences of crowded (nondiscriminable) symbols with their respective monetary outcomes (reward or punishment). Overall, our study demonstrates that sensitivity to sequential regularities can arise through the nonconscious temporal integration of perceptual information.

Inferring the direction of implied motion depends on visual awareness.

Visual awareness of an event, object, or scene is, by essence, an integrated experience, whereby different visual features composing an object (e.g., orientation, color, shape) appear as an unified percept and are processed as a whole. Here, we tested in human observers whether perceptual integration of static motion cues depends on awareness by measuring the capacity to infer the direction of motion implied by a static visible or invisible image under continuous flash suppression. Using measures of directional adaptation, we found that visible but not invisible implied motion adaptors biased the perception of real motion probes. In a control experiment, we found that invisible adaptors implying motion primed the perception of subsequent probes when they were identical (i.e., repetition priming), but not when they only shared the same direction (i.e., direction priming). Furthermore, using a model of visual processing, we argue that repetition priming effects are likely to arise as early as in the primary visual cortex. We conclude that although invisible images implying motion undergo some form of nonconscious processing, visual awareness is necessary to make inferences about motion direction.

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.

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.

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.

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.