Explaining distortions in metacognition with an attractor network model of decision uncertainty

Metacognition is the ability to reflect on, and evaluate, our cognition and behaviour. Distortions in metacognition are common in mental health disorders, though the neural underpinnings of such dysfunction are unknown. One reason for this is that models of key components of metacognition, such as decision confidence, are generally specified at an algorithmic or process level. While such models can be used to relate brain function to psychopathology, they are difficult to map to a neurobiological mechanism. Here, we develop a biologically-plausible model of decision uncertainty in an attempt to bridge this gap. We first relate the model’s uncertainty in perceptual decisions to standard metrics of metacognition, namely mean confidence level (bias) and the accuracy of metacognitive judgments (sensitivity). We show that dissociable shifts in metacognition are associated with isolated disturbances at higher-order levels of a circuit associated with self-monitoring, akin to neuropsychological findings that highlight the detrimental effect of prefrontal brain lesions on metacognitive performance. Notably, we are able to account for empirical confidence judgements by fitting the parameters of our biophysical model to first-order performance data, specifically choice and response times. Lastly, in a reanalysis of existing data we show that self-reported mental health symptoms relate to disturbances in an uncertainty-monitoring component of the network. By bridging a gap between a biologically-plausible model of confidence formation and observed disturbances of metacognition in mental health disorders we provide a first step towards mapping theoretical constructs of metacognition onto dynamical models of decision uncertainty. In doing so, we provide a computational framework for modelling metacognitive performance in settings where access to explicit confidence reports is not possible.     

Relating Pupil Dilation and Metacognitive Confidence during Auditory Decision-Making

The sources of evidence contributing to metacognitive assessments of confidence in decision-making remain unclear. Previous research has shown that pupil dilation is related to the signaling of uncertainty in a variety of decision tasks. Here we ask whether pupil dilation is also related to metacognitive estimates of confidence. Specifically, we measure the relationship between pupil dilation and confidence during an auditory decision task using a general linear model approach to take into account delays in the pupillary response. We found that pupil dilation responses track the inverse of confidence before but not after a decision is made, even when controlling for stimulus difficulty. In support of an additional post-decisional contribution to the accuracy of confidence judgments, we found that participants with better metacognitive ability – that is, more accurate appraisal of their own decisions – showed a tighter relationship between post-decisional pupil dilation and confidence. Together our findings show that a physiological index of uncertainty, pupil dilation, predicts both confidence and metacognitive accuracy for auditory decisions.     

Paradoxical Interaction between Ocular Activity,Perception, and Decision Confidence at the Threshold of Vision

In humans and some other species perceptual decision-making is complemented by the ability to make confidence judgements about the certainty of sensory evidence. While both forms of decision process have been studied empirically, the precise relationship between them remains poorly understood. We performed an experiment that combined a perceptual decision-making task (identifying the category of a faint visual stimulus) with a confidence-judgement task (wagering on the accuracy of each perceptual decision). The visual stimulation paradigm required steady fixation, so we used eye-tracking to control for stray eye movements. Our data analyses revealed an unexpected and counterintuitive interaction between the steadiness of fixation (prior to and during stimulation), perceptual decision making, and post-decision wagering: greater variability in gaze direction during fixation was associated with significantly increased visual-perceptual sensitivity, but significantly decreased reliability of confidence judgements. The latter effect could not be explained by a simple change in overall confidence (i.e. a criterion artifact), but rather was tied to a change in the degree to which high wagers predicted correct decisions (i.e. the sensitivity of the confidence judgement). We found no evidence of a differential change in pupil diameter that could account for the effect and thus our results are consistent with fixational eye movements being the relevant covariate. However, we note that small changes in pupil diameter can sometimes cause artefactual fluctuations in measured gaze direction and this possibility could not be fully ruled out. In either case, our results suggest that perceptual decisions and confidence judgements can be processed independently and point toward a new avenue of research into the relationship between them.     

Neuronal correlates of metacognition in primate frontal cortex

Humans are metacognitive: they monitor and control their cognition. Our hypothesis was that neuronal correlates of metacognition reside in the same brain areas responsible for cognition, including frontal cortex. Recent work demonstrated that nonhuman primates are capable of metacognition, so we recorded from single neurons in the frontal eye field, dorsolateral prefrontal cortex, and supplementary eye field of monkeys (Macaca mulatta) that performed a metacognitive visual-oculomotor task. The animals made a decision and reported it with a saccade, but received no immediate reward or feedback. Instead, they had to monitor their decision and bet whether it was correct. Activity was correlated with decisions and bets in all three brain areas, but putative metacognitive activity that linked decisions to appropriate bets occurred exclusively in the SEF. Our results offer a survey of neuronal correlates of metacognition and implicate the SEF in linking cognitive functions over short periods of time.     

Judgements of agency in schizophrenia: an impairment in autonoetic metacognition

We investigated judgements of agency in participants with schizophrenia and healthy controls. Participants engaged in a computer game in which they attempted to touch downward falling Xs and avoid touching Os. On some trials, participants were objectively in perfect control. On other trials, they were objectively not in complete control because the movement of the cursor on the screen was distorted with respect to the position of the mouse by random noise (turbulence), or it was lagged by 250 or 500 ms. Participants made metacognitive judgements of agency as well as judgements of performance. Control participants' judgements of agency were affected by the turbulence and lag variables-indicating that they knew they were objectively not in control in those conditions, and they were also influenced by their assessments of performance. The patients also used their assessments of performance but neither turbulence nor lag affected their judgements of agency. This indicated an impairment in agency monitoring. The patients, unlike the healthy controls, used only publically available external cues about performance in making judgements of 'agency' and did not rely on any additional access to internal self-relevant cues that were diagnostic in indicating whether or not they were, in fact, in control.     

Error-related negativity predicts reinforcement learning and conflict biases

The error-related negativity (ERN) is an electrophysiological marker thought to reflect changes in dopamine when participants make errors in cognitive tasks. Our computational model further predicts that larger ERNs should be associated with better learning to avoid maladaptive responses. Here we show that participants who avoided negative events had larger ERNs than those who were biased to learn more from positive outcomes. We also tested for effects of response conflict on ERN magnitude. While there was no overall effect of conflict, positive learners had larger ERNs when having to choose among two good options (win/win decisions) compared with two bad options (lose/lose decisions), whereas negative learners exhibited the opposite pattern. These results demonstrate that the ERN predicts the degree to which participants are biased to learn more from their mistakes than their correct choices and clarify the extent to which it indexes decision conflict.     

Metacognitive Confidence Increases with,but Does Not Determine,Visual Perceptual Learning

While perceptual learning increases objective sensitivity, the effects on the constant interaction of the process of perception and its metacognitive evaluation have been rarely investigated. Visual perception has been described as a process of probabilistic inference featuring metacognitive evaluations of choice certainty. For visual motion perception in healthy, naive human subjects here we show that perceptual sensitivity and confidence in it increased with training. The metacognitive sensitivity–estimated from certainty ratings by a bias-free signal detection theoretic approach–in contrast, did not. Concomitant 3Hz transcranial alternating current stimulation (tACS) was applied in compliance with previous findings on effective high-low cross-frequency coupling subserving signal detection. While perceptual accuracy and confidence in it improved with training, there were no statistically significant tACS effects. Neither metacognitive sensitivity in distinguishing between their own correct and incorrect stimulus classifications, nor decision confidence itself determined the subjects’ visual perceptual learning. Improvements of objective performance and the metacognitive confidence in it were rather determined by the perceptual sensitivity at the outset of the experiment. Post-decision certainty in visual perceptual learning was neither independent of objective performance, nor requisite for changes in sensitivity, but rather covaried with objective performance. The exact functional role of metacognitive confidence in human visual perception has yet to be determined.     

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.     

The neural basis of metacognitive ability

Ability in various cognitive domains is often assessed by measuring task performance, such as the accuracy of a perceptual categorization. A similar analysis can be applied to metacognitive reports about a task to quantify the degree to which an individual is aware of his or her success or failure. Here, we review the psychological and neural underpinnings of metacognitive accuracy, drawing on research in memory and decision-making. These data show that metacognitive accuracy is dissociable from task performance and varies across individuals. Convergent evidence indicates that the function of the rostral and dorsal aspect of the lateral prefrontal cortex (PFC) is important for the accuracy of retrospective judgements of performance. In contrast, prospective judgements of performance may depend upon medial PFC. We close with a discussion of how metacognitive processes relate to concepts of cognitive control, and propose a neural synthesis in which dorsolateral and anterior prefrontal cortical subregions interact with interoceptive cortices (cingulate and insula) to promote accurate judgements of performance.     

A metamemory perspective on odor naming and identification

A metacognitive perspective is utilized to elucidate why it is so difficult to name common odors and what characterizes the subjective knowledge people have about their actual odor knowledge. Odor-naming failures are often accompanied by strong feelings of knowing (FOK) or feelings of imminent retrieval of what it is that smells. The paper's two experiments investigate FOK judgements and tip of the tongue (TOT) experiences for odor and person names. The data indicate that our inability to correctly name odors are typically not due to the often proposed uniquely poor association between odors and their proper names, but rather due to failures to identify the odors, that is, failures to know 'what it is'. It was also found that (i) TOT experiences are very unusual for odor names and more so than for person names; (ii) FOK judgements about odor names are significantly less predictive of later retrieval than equivalent judgements about names of persons; (iii) FOK judgements were highly correlated with the familiarity of the cue (odor or picture of famous person), rendering some support for the idea that FOK judgements are based on the perceived familiarity of the cue triggering the FOK; and (iv) the idea that FOK judgements are based on the amount of available information about the sought-for memory (accessibility theory) was also supported.     

Risk Assessment in Navy Deployment Toxicology

The risk assessment process is a critical function for deployment toxicology research. It is essential to the decision making process related to establishing risk reduction procedures and for formulating appropriate exposure levels to protect naval personnel from potentially hazardous chemicals in the military that could result in a reduction in readiness operations. These decisions must be based on quality data from well-planned laboratory animal studies that guide the judgements, which result in effective risk characterization and risk management. The process of risk assessment in deployment toxicology essentially uses the same principles as civilian risk assessment, but adds activities essential to the military mission, including intended and unintended exposure to chemicals and chemical mixtures. Risk assessment and Navy deployment toxicology data are integrated into a systematic and well-planned approach to the organization of scientific information. The purpose of this paper is to outline the analytical framework used to develop strategies to protect the health of deployed Navy forces.     

Visual clutter causes high-magnitude errors

Perceptual decisions are often made in cluttered environments, where a target may be confounded with competing “distractor” stimuli. Although many studies and theoretical treatments have highlighted the effect of distractors on performance, it remains unclear how they affect thequality of perceptual decisions. Here we show that perceptual clutter leads not only to an increase in judgment errors, but also to an increase in perceived signal strength and decision confidence on erroneous trials. Observers reported simultaneously the direction and magnitude of the tilt of a target grating presented either alone, or together with vertical distractor stimuli. When presented in isolation, observers perceived isolated targets as only slightly tilted on error trials, and had little confidence in their decision. When the target was embedded in distractors, however, they perceived it to be strongly tilted on error trials, and had high confidence of their (erroneous) decisions. The results are well explained by assuming that the observers' internal representation of stimulus orientation arises from a nonlinear combination of the outputs of independent noise-perturbed front-end detectors. The implication that erroneous perceptual decisions in cluttered environments are made with high confidence has many potential practical consequences, and may be extendable to decision-making in general.     

A computational framework for the study of confidence in humans and animals

Confidence judgements, self-assessments about the quality of a subject's knowledge, are considered a central example of metacognition. Prima facie, introspection and self-report appear the only way to access the subjective sense of confidence or uncertainty. Contrary to this notion, overt behavioural measures can be used to study confidence judgements by animals trained in decision-making tasks with perceptual or mnemonic uncertainty. Here, we suggest that a computational approach can clarify the issues involved in interpreting these tasks and provide a much needed springboard for advancing the scientific understanding of confidence. We first review relevant theories of probabilistic inference and decision-making. We then critically discuss behavioural tasks employed to measure confidence in animals and show how quantitative models can help to constrain the computational strategies underlying confidence-reporting behaviours. In our view, post-decision wagering tasks with continuous measures of confidence appear to offer the best available metrics of confidence. Since behavioural reports alone provide a limited window into mechanism, we argue that progress calls for measuring the neural representations and identifying the computations underlying confidence reports. We present a case study using such a computational approach to study the neural correlates of decision confidence in rats. This work shows that confidence assessments may be considered higher order, but can be generated using elementary neural computations that are available to a wide range of species. Finally, we discuss the relationship of confidence judgements to the wider behavioural uses of confidence and uncertainty.     

Metacognition for Spelling in Higher Education Students with Dyslexia: Is There Evidence for the Dual Burden Hypothesis?

We examined whether academic and professional bachelor students with dyslexia are able to compensate for their spelling deficits with metacognitive experience. Previous research suggested that students with dyslexia may suffer from a dual burden. Not only do they perform worse on spelling but in addition they are not as fully aware of their difficulties as their peers without dyslexia. According to some authors, this is the result of a worse feeling of confidence, which can be considered as a form of metacognition (metacognitive experience). We tried to isolate this metacognitive experience by asking 100 students with dyslexia and 100 matched control students to rate their feeling of confidence in a word spelling task and a proofreading task. Next, we used Signal Detection Analysis to disentangle the effects of proficiency and criterion setting. We found that students with dyslexia showed lower proficiencies but not suboptimal response biases. They were as good at deciding when they could be confident or not as their peers without dyslexia. They just had more cases in which their spelling was wrong. We conclude that the feeling of confidence in our students with dyslexia is as good as in their peers without dyslexia. These findings go against the Dual Burden theory (Krüger & Dunning, 1999), which assumes that people with a skills problem suffer twice as a result of insufficiently developed metacognitive competence. As a result, there is no gain to be expected from extra training of this metacognitive experience in higher education students with dyslexia.     

A Bayesian Attractor Model for Perceptual Decision Making

Even for simple perceptual decisions, the mechanisms that the brain employs are still under debate. Although current consensus states that the brain accumulates evidence extracted from noisy sensory information, open questions remain about how this simple model relates to other perceptual phenomena such as flexibility in decisions, decision-dependent modulation of sensory gain, or confidence about a decision. We propose a novel approach of how perceptual decisions are made by combining two influential formalisms into a new model. Specifically, we embed an attractor model of decision making into a probabilistic framework that models decision making as Bayesian inference. We show that the new model can explain decision making behaviour by fitting it to experimental data. In addition, the new model combines for the first time three important features: First, the model can update decisions in response to switches in the underlying stimulus. Second, the probabilistic formulation accounts for top-down effects that may explain recent experimental findings of decision-related gain modulation of sensory neurons. Finally, the model computes an explicit measure of confidence which we relate to recent experimental evidence for confidence computations in perceptual decision tasks.     

An ERP Analysis of Recognition and Categorization Decisions in a Prototype-Distortion Task

Background

Theories of categorization make different predictions about the underlying processes used to represent categories. Episodic theories suggest that categories are represented in memory by storing previously encountered exemplars in memory. Prototype theories suggest that categories are represented in the form of a prototype independently of memory. A number of studies that show dissociations between categorization and recognition are often cited as evidence for the prototype account. These dissociations have compared recognition judgements made to one set of items to categorization judgements to a different set of items making a clear interpretation difficult. Instead of using different stimuli for different tests this experiment compares the processes by which participants make decisions about category membership in a prototype-distortion task and with recognition decisions about the same set of stimuli by examining the Event Related Potentials (ERPs) associated with them.

Method

Sixty-three participants were asked to make categorization or recognition decisions about stimuli that either formed an artificial category or that were category non-members. We examined the ERP components associated with both kinds of decision for pre-exposed and control participants.

Conclusion

In contrast to studies using different items we observed no behavioural differences between the two kinds of decision; participants were equally able to distinguish category members from non-members, regardless of whether they were performing a recognition or categorisation judgement. Interestingly, this did not interact with prior-exposure. However, the ERP data demonstrated that the early visual evoked response that discriminated category members from non-members was modulated by which judgement participants performed and whether they had been pre-exposed to category members. We conclude from this that any differences between categorization and recognition reflect differences in the information that participants focus on in the stimuli to make the judgements at test, rather than any differences in encoding or process.     

Group decision making in fission-fusion societies: evidence from two-field experiments in Bechstein's bats

Group decisions are required when group coordination is beneficial, but individuals can choose between alternatives. Despite the increased interest in animal group decision making, there is a lack of experimental field studies that investigate how animals with conflicting information make group decisions. In particular, no field studies have considered the influence of fission-fusion behaviour (temporary splitting into subgroups) on group decisions. We studied group decision making in two wild Bechstein's bat colonies, which are fission-fusion societies of stable individual composition. Since they frequently switch communal roosts, colony members must regularly make group decisions over where to roost. In the two-field experiments, we provided marked individuals with conflicting information about the suitability of potential roosts. We investigated whether conflicting information led to group decisions that followed a 'unanimous' or a 'majority' rule, or increased colony fission. Individual behaviour suggests that bats considered both their own information and the behaviour of others when deciding where to roost. Group decisions about communal roosts reflected the information available to a majority of the bats roosting together, but conflicting information led to an increased fission in one colony. Our results suggest that fission-fusion societies allow individuals to avoid majority decisions that are not in their favour.     

An initial ‘snapshot’ of sensory information biases the likelihood and speed of subsequent changes of mind

We often need to rapidly change our mind about perceptual decisions in order to account for new information and correct mistakes. One fundamental, unresolved question is whether information processed prior to a decision being made (‘pre-decisional information’) has any influence on the likelihood and speed with which that decision is reversed. We investigated this using a luminance discrimination task in which participants indicated which of two flickering greyscale squares was brightest. Following an initial decision, the stimuli briefly remained on screen, and participants could change their response. Using psychophysical reverse correlation, we examined how moment-to-moment fluctuations in stimulus luminance affected participants’ decisions. This revealed that the strength of even the very earliest (pre-decisional) evidence was associated with the likelihood and speed of later changes of mind. To account for this effect, we propose an extended diffusion model in which an initial ‘snapshot’ of sensory information biases ongoing evidence accumulation.     

Epidemiology needs more interdisciplinary teams with expertise in molecular systematics,public health and food safety

What are considered fundamental principles within the Willi Hennig Society and published in their journal are not always fully appreciated by many other biological fields that have not been schooled in these disciplines of systematics principles and the reasons for why these principles are important (Wenzel, Cladistics, 2020, in press). Natural history museums and their associated programs have been a traditional source of the dissemination and training on the uses of phylogenetic systematics. Systematists should do more to expand these interdisciplinary collaborations by reaching out and supporting their local and international collaborators in public health, food and water safety, and other microbiology applications so that critical life-saving and timely phylogenetic-based decisions can be made.     

The neural basis of financial risk taking

Investors systematically deviate from rationality when making financial decisions, yet the mechanisms responsible for these deviations have not been identified. Using event-related fMRI, we examined whether anticipatory neural activity would predict optimal and suboptimal choices in a financial decision-making task. We characterized two types of deviations from the optimal investment strategy of a rational risk-neutral agent as risk-seeking mistakes and risk-aversion mistakes. Nucleus accumbens activation preceded risky choices as well as risk-seeking mistakes, while anterior insula activation preceded riskless choices as well as risk-aversion mistakes. These findings suggest that distinct neural circuits linked to anticipatory affect promote different types of financial choices and indicate that excessive activation of these circuits may lead to investing mistakes. Thus, consideration of anticipatory neural mechanisms may add predictive power to the rational actor model of economic decision making.