Metacognition as a window into subjective affective experience.

When patients seek professional help for mental disorders, they often do so because of troubling subjective affective experiences. While these subjective states are at the center of the patient's symptomatology, scientific tools for studying them and their cognitive antecedents are limited. Here, we explore the use of concepts and analytic tools from the science of consciousness, a field of research that has faced similar challenges in having to develop robust empirical methods for addressing a phenomenon that has been considered difficult to pin down experimentally. One important strand is the operationalization of some relevant processes in terms of metacognition and confidence ratings, which can be rigorously studied in both humans and animals. By assessing subjective experience with similar approaches, we hope to develop new scientific approaches for studying affective processes and promoting psychological resilience in the face of debilitating emotional experiences.

Putting the "mental" back in "mental disorders": a perspective from research on fear and anxiety.

Mental health problems often involve clusters of symptoms that include subjective (conscious) experiences as well as behavioral and/or physiological responses. Because the bodily responses are readily measured objectively, these have come to be emphasized when developing treatments and assessing their effectiveness. On the other hand, the subjective experience of the patient reported during a clinical interview is often viewed as a weak correlate of psychopathology. To the extent that subjective symptoms are related to the underlying problem, it is often assumed that they will be taken care of if the more objective behavioral and physiological symptoms are properly treated. Decades of research on anxiety disorders, however, show that behavioral and physiological symptoms do not correlate as strongly with subjective experiences as is typically assumed. Further, the treatments developed using more objective symptoms as a marker of psychopathology have mostly been disappointing in effectiveness. Given that "mental" disorders are named for, and defined by, their subjective mental qualities, it is perhaps not surprising, in retrospect, that treatments that have sidelined mental qualities have not been especially effective. These negative attitudes about subjective experience took root in psychiatry and allied fields decades ago when there were few avenues for scientifically studying subjective experience. Today, however, cognitive neuroscience research on consciousness is thriving, and offers a viable and novel scientific approach that could help achieve a deeper understanding of mental disorders and their treatment.

A little history goes a long way toward understanding why we study consciousness the way we do today.

Consciousness is currently a thriving area of research in psychology and neuroscience. While this is often attributed to events that took place in the early 1990s, consciousness studies today are a continuation of research that started in the late 19th century and that continued throughout the 20th century. From the beginning, the effort built on studies of animals to reveal basic principles of brain organization and function, and of human patients to gain clues about consciousness itself. Particularly important and our focus here is research in the 1950s, 1960s, and 1970s involving three groups of patients-amnesia, split brain, and blindsight. Across all three groups, a similar pattern of results was found-the patients could respond appropriately to stimuli that they denied seeing (or in the case of amnesiacs, having seen before). These studies paved the way for the current wave of research on consciousness. The field is, in fact, still grappling with the implications of the findings showing that the ability to consciously know and report the identity of a visual stimulus can be dissociated in the brain from the mechanisms that underlie the ability to behave in a meaningful way to the same stimulus.

Variable Statistical Structure of Neuronal Spike Trains in Monkey Superior Colliculus.

Popular models of decision-making propose that noisy sensory evidence accumulates until reaching a bound. Behavioral evidence as well as trial-averaged ramping of neuronal activity in sensorimotor regions of the brain support this idea. However, averaging activity across trials can mask other processes, such as rapid shifts in decision commitment, calling into question the hypothesis that evidence accumulation is encoded by delay period activity of individual neurons. We mined two sets of data from experiments in four monkeys in which we recorded from superior colliculus neurons during two different decision-making tasks and a delayed saccade task. We applied second-order statistical measures and spike train simulations to determine whether spiking statistics were similar or different in the different tasks and monkeys, despite similar trial-averaged activity across tasks and monkeys. During a motion direction discrimination task, single-trial delay period activity behaved statistically consistent with accumulation. During an orientation detection task, the activity behaved superficially like accumulation, but statistically consistent with stepping. Simulations confirmed both findings. Importantly, during a simple saccade task, with similar trial-averaged activity, neither process explained spiking activity, ruling out interpretations based on differences in attention, reward, or motor planning. These results highlight the need for exploring single-trial spiking dynamics to understand cognitive processing and raise the interesting hypothesis that the superior colliculus participates in different aspects of decision-making depending on task differences.SIGNIFICANCE STATEMENT How are decisions based on sensory information transformed into actions? We report that single-trial neuronal activity dynamics in the superior colliculus of monkeys show differences in decision-making tasks depending on task idiosyncrasies and requirements and despite similar trial-averaged ramping activity. These results highlight the importance of exploring single-trial spiking dynamics to understand cognitive processing and raise the interesting hypothesis that the superior colliculus participates in different aspects of decision-making depending on task requirements.

Tuned inhibition in perceptual decision-making circuits can explain seemingly suboptimal confidence behavior.

Current dominant views hold that perceptual confidence reflects the probability that a decision is correct. Although these views have enjoyed some empirical support, recent behavioral results indicate that confidence and the probability of being correct can be dissociated. An alternative hypothesis suggests that confidence instead reflects the magnitude of evidence in favor of a decision while being relatively insensitive to the evidence opposing the decision. We considered how this alternative hypothesis might be biologically instantiated by developing a simple neural network model incorporating a known property of sensory neurons: tuned inhibition. The key idea of the model is that the level of inhibition that each accumulator unit receives from units with the opposite tuning preference, i.e. its inhibition 'tuning', dictates its contribution to perceptual decisions versus confidence judgments, such that units with higher tuned inhibition (computing relative evidence for different perceptual interpretations) determine perceptual discrimination decisions, and units with lower tuned inhibition (computing absolute evidence) determine confidence. We demonstrate that this biologically plausible model can account for several counterintuitive findings reported in the literature where confidence and decision accuracy dissociate. By comparing model fits, we further demonstrate that a full complement of behavioral data across several previously published experimental results-including accuracy, reaction time, mean confidence, and metacognitive sensitivity-is best accounted for when confidence is computed from units without, rather than units with, tuned inhibition. Finally, we discuss predictions of our results and model for future neurobiological studies. These findings suggest that the brain has developed and implements this alternative, heuristic theory of perceptual confidence computation by relying on the diversity of neural resources available.

Real-Time Functional MRI in the Treatment of Mental Health Disorders.

Multiple mental disorders have been associated with dysregulation of precise brain processes. However, few therapeutic approaches can correct such specific patterns of brain activity. Since the late 1960s and early 1970s, many researchers have hoped that this feat could be achieved by closed-loop brain imaging approaches, such as neurofeedback, that aim to modulate brain activity directly. However, neurofeedback never gained mainstream acceptance in mental health, in part due to methodological considerations. In this review, we argue that, when contemporary methodological guidelines are followed, neurofeedback is one of the few intervention methods in psychology that can be assessed in double-blind placebo-controlled trials. Furthermore, using new advances in machine learning and statistics, it is now possible to target very precise patterns of brain activity for therapeutic purposes. We review the recent literature in functional magnetic resonance imaging neurofeedback and discuss current and future applications to mental health.

Transcranial magnetic stimulation alters multivoxel patterns in the absence of overall activity changes.

Transcranial magnetic stimulation (TMS) has become one of the major tools for establishing the causal role of specific brain regions in perceptual, motor, and cognitive processes. Nevertheless, a persistent limitation of the technique is the lack of clarity regarding its precise effects on neural activity. Here, we examined the effects of TMS intensity and frequency on concurrently recorded blood-oxygen-level-dependent (BOLD) signals at the site of stimulation. In two experiments, we delivered TMS to the dorsolateral prefrontal cortex in human subjects of both sexes. In Experiment 1, we delivered a series of pulses at high (100% of motor threshold) or low (50% of motor threshold) intensity, whereas, in Experiment 2, we always used high intensity but delivered stimulation at four different frequencies (5, 8.33, 12.5, and 25 Hz). We found that the TMS intensity and frequency could be reliably decoded using multivariate analysis techniques even though TMS had no effect on the overall BOLD activity at the site of stimulation in either experiment. These results provide important insight into the mechanisms through which TMS influences neural activity.

Multivoxel pattern analysis reveals dissociations between subjective fear and its physiological correlates.

In studies of anxiety and other affective disorders, objectively measured physiological responses have commonly been used as a proxy for measuring subjective experiences associated with pathology. However, this commonly adopted "biosignal" approach has recently been called into question on the grounds that subjective experiences and objective physiological responses may dissociate. We performed machine-learning-based analyses on functional magnetic resonance imaging (fMRI) data to assess this issue in the case of fear. Although subjective fear and objective physiological responses were correlated in general, the respective whole-brain multivoxel decoders for the two measures were different. Some key brain regions such as the amygdala and insula appear to be primarily involved in the prediction of physiological reactivity, whereas some regions previously associated with metacognition and conscious perception, including some areas in the prefrontal cortex, appear to be primarily predictive of the subjective experience of fear. The present findings are in support of the recent call for caution in assuming a one-to-one mapping between subjective sufferings and their putative biosignals, despite the clear advantages in the latter's being objectively and continuously measurable in physiological terms.

Attention Drifting In and Out: The Boredom Feedback Model.

We synthesize established and emerging research to propose a feedback process model that explicates key antecedents, experiences, and consequences of the emotion boredom. The proposed Boredom Feedback Model posits that the dynamic process of boredom resembles a feedback loop that centers on attention shifts instigated by inadequate attentional engagement. Inadequate attentional engagement is a discrepancy between desired and actual levels of attentional engagement and is a product of external and internal influences, reflected in objective resources and cognitive appraisals. The model sheds light on several essential yet unresolved puzzles in the literature, including how people learn to cope with boredom, how to understand the relation between self-control and boredom, how the roles of attention and meaning in boredom can be integrated, why boredom is associated with both high- and low-arousal negative emotions, and what contributes to chronic boredom. The model offers testable hypotheses for future research.

Superior colliculus neuronal ensemble activity signals optimal rather than subjective confidence.

Recent studies suggest that neurons in sensorimotor circuits involved in perceptual decision-making also play a role in decision confidence. In these studies, confidence is often considered to be an optimal readout of the probability that a decision is correct. However, the information leading to decision accuracy and the report of confidence often covaried, leaving open the possibility that there are actually two dissociable signal types in the brain: signals that correlate with decision accuracy (optimal confidence) and signals that correlate with subjects' behavioral reports of confidence (subjective confidence). We recorded neuronal activity from a sensorimotor decision area, the superior colliculus (SC) of monkeys, while they performed two different tasks. In our first task, decision accuracy and confidence covaried, as in previous studies. In our second task, we implemented a motion discrimination task with stimuli that were matched for decision accuracy but produced different levels of confidence, as reflected by behavioral reports. We used a multivariate decoder to predict monkeys' choices from neuronal population activity. As in previous studies on perceptual decision-making mechanisms, we found that neuronal decoding performance increased as decision accuracy increased. However, when decision accuracy was matched, performance of the decoder was similar between high and low subjective confidence conditions. These results show that the SC likely signals optimal decision confidence similar to previously reported cortical mechanisms, but is unlikely to play a critical role in subjective confidence. The results also motivate future investigations to determine where in the brain signals related to subjective confidence reside.

Towards an unconscious neural reinforcement intervention for common fears.

Can "hardwired" physiological fear responses (e.g., for spiders and snakes) be reprogramed unconsciously in the human brain? Currently, exposure therapy is among the most effective treatments for anxiety disorders, but this intervention is subjectively aversive to patients, causing many to drop out of treatment prematurely. Here we introduce a method to bypass the subjective unpleasantness in conscious exposure, by directly pairing monetary reward with unconscious occurrences of decoded representations of naturally feared animals in the brain. To decode physiological fear representations without triggering excessively aversive reactions, we capitalize on recent advancements in functional magnetic resonance imaging decoding techniques, and use a method called hyperalignment to infer the relevant representations of feared animals for a designated participant based on data from other "surrogate" participants. In this way, the procedure completely bypasses the need for a conscious encounter with feared animals. We demonstrate that our method can lead to reliable reductions in physiological fear responses, as measured by skin conductance as well as amygdala hemodynamic activity. Not only do these results raise the intriguing possibility that naturally occurring fear responses can be "reprogrammed" outside of conscious awareness, importantly, they also create the rare opportunity to rigorously test a psychological intervention of this nature in a double-blind, placebo-controlled fashion. This may pave the way for a new approach combining the appealing rationale and proven efficacy of conventional psychotherapy with the rigor and leverage of clinical neuroscience.

Spatiotemporal dynamics of brightness coding in human visual cortex revealed by the temporal context effect.

Human visual perception is modulated by both temporal and spatial contexts. One type of modulation is apparent in the temporal context effect (TCE): In the presence of a constant luminance patch (a long flash), the perceived brightness of a short flash increases monotonically with onset asynchrony. The aim of the current study was to delineate the neural correlates of this illusory effect, particularly focusing on its dynamic neural representation among visual cortical areas. We reconstructed sources of magnetoencephalographic (MEG) data recorded from observers (6 male and 9 female human adults) experiencing the TCE. Together with retinotopic mapping, signals from different occipital lobe areas were extracted to investigate whether different visual areas have differential representation of the onset vs. offset synchronized short flashes. From the data, TCE related responses were observed in LO and V4 in the time window of 200-250 m s, while neuronal responses to physical luminances were observed in the early time window at around 100 m s across early visual cortex, such as V1 and V2, also in V4 and VO. Based on these findings, we suggest that two distinct processes might be involved in brightness coding: one bottom-up process which is stimulus energy driven and responds fast, and another process which may be broadly characterized as top-down or lateral, is context driven, and responds slower. For both processes, we found that V4 might play a critical role in dynamically integrating luminances into brightness perception, a finding that is consistent with the view of V4 as a bottom-up and top-down integration complex.

Domain-General and Domain-Specific Patterns of Activity Supporting Metacognition in Human Prefrontal Cortex.

Metacognition is the capacity to evaluate the success of one's own cognitive processes in various domains; for example, memory and perception. It remains controversial whether metacognition relies on a domain-general resource that is applied to different tasks or if self-evaluative processes are domain specific. Here, we investigated this issue directly by examining the neural substrates engaged when metacognitive judgments were made by human participants of both sexes during perceptual and memory tasks matched for stimulus and performance characteristics. By comparing patterns of fMRI activity while subjects evaluated their performance, we revealed both domain-specific and domain-general metacognitive representations. Multivoxel activity patterns in anterior prefrontal cortex predicted levels of confidence in a domain-specific fashion, whereas domain-general signals predicting confidence and accuracy were found in a widespread network in the frontal and posterior midline. The demonstration of domain-specific metacognitive representations suggests the presence of a content-rich mechanism available to introspection and cognitive control.SIGNIFICANCE STATEMENT We used human neuroimaging to investigate processes supporting memory and perceptual metacognition. It remains controversial whether metacognition relies on a global resource that is applied to different tasks or if self-evaluative processes are specific to particular tasks. Using multivariate decoding methods, we provide evidence that perceptual- and memory-specific metacognitive representations coexist with generic confidence signals. Our findings reconcile previously conflicting results on the domain specificity/generality of metacognition and lay the groundwork for a mechanistic understanding of metacognitive judgments.

Causal Evidence for Mnemonic Metacognition in Human Precuneus.

Metacognition is the capacity to introspectively monitor and control one's own cognitive processes. Previous anatomical and functional neuroimaging findings implicated the important role of the precuneus in metacognition processing, especially during mnemonic tasks. However, the issue of whether this medial parietal cortex is a domain-specific region that supports mnemonic metacognition remains controversial. Here, we focally disrupted this parietal area with repetitive transcranial magnetic stimulation in healthy human participants of both sexes, seeking to ascertain its functional necessity for metacognition in memory versus perceptual decisions. Perturbing precuneal activity selectively impaired metacognitive efficiency of temporal-order memory judgment, but not perceptual discrimination. Moreover, the correlation in individuals' metacognitive efficiency between domains disappeared when the precuneus was perturbed. Together, these findings provide evidence reinforcing the notion that the precuneal region plays an important role in mediating metacognition of episodic memory retrieval.SIGNIFICANCE STATEMENT Theories on the neural basis of metacognition have thus far been largely centered on the role of the prefrontal cortex. Here we refined the theoretical framework through characterizing a unique precuneal involvement in mnemonic metacognition with a noninvasive but inferentially powerful method: transcranial magnetic stimulation. By quantifying metacognitive efficiency across two distinct domains (memory vs perception) that are matched for stimulus characteristics, we reveal an instrumental role of the precuneus in mnemonic metacognition. This causal evidence corroborates ample clinical reports that parietal lobe lesions often produce inaccurate self-reports of confidence in memory recollection and establish the precuneus as a nexus for the introspective ability to evaluate the success of memory judgment in humans.

Human brain responses to gustatory and food stimuli: A meta-evaluation of neuroimaging meta-analyses.

Multiple neuroimaging meta-analyses have been published concerning gustation, food and taste. A meta-evaluation of these meta-analyses was conducted to qualitatively evaluate the presented evidence. A systematic search was done using multiple databases, in which no restriction was placed on participants and nature of interventions (stimuli vs control). Twenty-three meta-analyses were identified and analyzed. All of them have met 4-9 criteria, out of 11, from the modified checklist constructed by Müller et al. (2018), which implied moderate to high quality of evidence. One of the concerns we found was that no meta-analysis surveyed had been explicitly pre-registered. Also, only three meta-analyses (13.0%) provided clear explanation of how they accounted for sample overlap. Only six meta-analyses (26.1%) explicitly described how they double checked the data. Only two of the 20 meta-analyses (10.0%) using GingerALE software used both the debugged version (v2.3.6) as well as the recommended cluster-level inference with familywise error rate correction. Overall, meta-analyses are increasingly adopting more stringent statistical thresholds, but unfortunately not larger number of studies contained in the analyses.

How the Brain Converts Negative Evaluation into Performance Facilitation.

Surpassing negative evaluation is a recurrent theme of success stories. Yet, there is little evidence supporting the counterintuitive idea that negative evaluation might not only motivate people, but also enhance performance. To address this question, we designed a task that required participants to decide whether taking up a risky challenge after receiving positive or negative evaluations from independent judges. Participants believed that these evaluations were based on their prior performance on a related task. Results showed that negative evaluation caused a facilitation in performance. Concurrent functional magnetic resonance imaging revealed that the motivating effect of negative evaluation was represented in the insula and striatum, while the performance boost was associated with functional positive connectivity between the insula and a set of brain regions involved in goal-directed behavior and the orienting of attention. These findings provide new insight into the neural representation of negative evaluation-induced facilitation.

Should a Few Null Findings Falsify Prefrontal Theories of Conscious Perception?

Is activity in prefrontal cortex (PFC) critical for conscious perception? Major theories of consciousness make distinct predictions about the role of PFC, providing an opportunity to arbitrate between these views empirically. Here we address three common misconceptions: (1) PFC lesions do not affect subjective perception; (2) PFC activity does not reflect specific perceptual content; and (3) PFC involvement in studies of perceptual awareness is solely driven by the need to make reports required by the experimental tasks rather than subjective experience per se. These claims are incompatible with empirical findings, unless one focuses only on studies using methods with limited sensitivity. The literature highlights PFC's essential role in enabling the subjective experience in perception, contra the objective capacity to perform visual tasks; conflating the two can also be a source of confusion.Dual Perspectives Companion Paper: Are the Neural Correlates of Consciousness in the Front or in the Back of the Cerebral Cortex? Clinical and Neuroimaging Evidence, by Melanie Boly, Marcello Massimini, Naotsugu Tsuchiya, Bradley R. Postle, Christof Koch, and Giulio Tononi.

Limited Cognitive Resources Explain a Trade-Off between Perceptual and Metacognitive Vigilance.

Why do experimenters give subjects short breaks in long behavioral experiments? Whereas previous studies suggest it is difficult to maintain attention and vigilance over long periods of time, it is unclear precisely what mechanisms benefit from rest after short experimental blocks. Here, we evaluate decline in both perceptual performance and metacognitive sensitivity (i.e., how well confidence ratings track perceptual decision accuracy) over time and investigate whether characteristics of prefrontal cortical areas correlate with these measures. Whereas a single-process signal detection model predicts that these two forms of fatigue should be strongly positively correlated, a dual-process model predicts that rates of decline may dissociate. Here, we show that these measures consistently exhibited negative or near-zero correlations, as if engaged in a trade-off relationship, suggesting that different mechanisms contribute to perceptual and metacognitive decisions. Despite this dissociation, the two mechanisms likely depend on common resources, which could explain their trade-off relationship. Based on structural MRI brain images of individual human subjects, we assessed gray matter volume in the frontal polar area, a region that has been linked to visual metacognition. Variability of frontal polar volume correlated with individual differences in behavior, indicating the region may play a role in supplying common resources for both perceptual and metacognitive vigilance. Additional experiments revealed that reduced metacognitive demand led to superior perceptual vigilance, providing further support for this hypothesis. Overall, results indicate that during breaks between short blocks, it is the higher-level perceptual decision mechanisms, rather than lower-level sensory machinery, that benefit most from rest. SIGNIFICANCE STATEMENT: Perceptual task performance declines over time (the so-called vigilance decrement), but the relationship between vigilance in perception and metacognition has not yet been explored in depth. Here, we show that patterns in perceptual and metacognitive vigilance do not follow the pattern predicted by a previously suggested single-process model of perceptual and metacognitive decision making. We account for these findings by showing that regions of anterior prefrontal cortex (aPFC) previously associated with visual metacognition are also associated with perceptual vigilance. We also show that relieving metacognitive task demand improves perceptual vigilance, suggesting that aPFC may house a limited cognitive resource that contributes to both metacognition and perceptual vigilance. These findings advance our understanding of the mechanisms and dynamics of perceptual metacognition.

Superior colliculus signals decisions rather than confidence: analysis of single neurons.

Recent findings indicate that monkeys can report their confidence in perceptual decisions and that this information is encoded in neurons involved in making decisions, including the lateral intraparietal area (LIP) and the supplementary eye field (SEF). A key issue to consider when studying confidence is that decision accuracy often correlates with confidence reports; when we are performing well, we generally feel more confident. Expanding on work performed in humans, we designed a novel task for monkeys that dissociates perceptual information leading to decisions from perceptual information leading to confidence reports. Using this task, we recently showed that decoded ensemble activity recorded from the superior colliculus (SC) reflected decisions rather than confidence reports. However, our previous population level analysis collapsed over multiple SC neuronal types and therefore left open the possibility that first, individual discharge rates might encode information related to decision confidence, and second, different neuronal cell types within the SC might signal decision confidence independently of decision accuracy. We found that when decision accuracy and decision confidence covaried, modulation occurred primarily in neurons with prelude activity (buildup neurons). However, isolating decision confidence from decision accuracy uncovered that only a few, primarily buildup neurons showed signals correlating uniquely with decision confidence and the effect sizes were very small. Based on this work and our previous work using decoding methods, we conclude that neuronal signals for decision confidence, independent of decision accuracy, are unlikely to exist at the level of single or populations of neurons in the SC. Our results together with other recent work call into question normative models of confidence based on the optimal readout of decision signals. NEW & NOTEWORTHY Models of decision confidence suggest that our sense of confidence is an optimal readout of perceptual decision signals. Here, we report that a subcortical area, the superior colliculus (SC), contains neurons with activity that signal decisions and confidence in a task in which decision accuracy and confidence covary, similar to area lateral intraparietal area in cortex. The signals from SC occur primarily in the neurons with prelude activity (buildup neurons). However, in a task that dissociates decision accuracy from decision confidence, we find that only a few individual neurons express unique signals of confidence. These results call into question normative models of confidence based on optimal readout of perceptual decision signals.