Human VMPFC encodes early signatures of confidence in perceptual decisions.
ABSTRACT: Choice confidence, an individual's internal estimate of judgment accuracy, plays a critical role in adaptive behaviour, yet its neural representations during decision formation remain underexplored. Here, we recorded simultaneous EEG-fMRI while participants performed a direction discrimination task and rated their confidence on each trial. Using multivariate single-trial discriminant analysis of the EEG, we identified a stimulus-independent component encoding confidence, which appeared prior to subjects' explicit choice and confidence report, and was consistent with a confidence measure predicted by an accumulation-to-bound model of decision-making. Importantly, trial-to-trial variability in this electrophysiologically-derived confidence signal was uniquely associated with fMRI responses in the ventromedial prefrontal cortex (VMPFC), a region not typically associated with confidence for perceptual decisions. Furthermore, activity in the VMPFC was functionally coupled with regions of the frontal cortex linked to perceptual decision-making and metacognition. Our results suggest that the VMPFC holds an early confidence representation arising from decision dynamics, preceding and potentially informing metacognitive evaluation.
Project description:Visual metacognition-the introspection and evaluation of one's own visual perceptual processes-is measured through both decision confidence and "metacognitive efficiency." Metacognitive efficiency refers to an individual's ability to accurately judge incorrect and correct decisions through confidence ratings given their task performance. Previous imaging studies in humans and nonhuman primates reported widely distributed brain regions being involved in decision confidence and metacognition. However, the neural correlates of metacognition are remarkably inconsistent across studies concerning spatial outline. Therefore, this study investigates the neural correlates of visual metacognition by examining co-activation across regions that scale with visual decision confidence. We hypothesized that interacting processes of perceptual and metacognitive performance contribute to the arising decision confidence in distributed, but segregable co-activating brain regions. To test this hypothesis, we performed task-fMRI in healthy humans during a visual backward masking task with four-scale, post-decision confidence ratings. We measured blood oxygenation covariation patterns, which served as a physiological proxy for co-activation across brain regions. Decision confidence ratings and an individual's metacognitive efficiency served as behavioral measures for metacognition. We found three distinct co-activation clusters involved in decision confidence: the first included right-centered fronto-temporal-parietal regions, the second included left temporal and parietal regions, and the left basal forebrain (BF), and the third included cerebellar regions. The right fronto-temporal-parietal cluster including the supplementary eye field and the right basal forebrain showed stronger co-activation in subjects with higher metacognitive efficiency. Our results provide novel evidence for co-activation of widely distributed fronto-parieto-temporal regions involved in visual confidence. The supplementary eye field was the only region that activated for both decision confidence and metacognitive efficiency, suggesting the supplementary eye field plays a key role in visual metacognition. Our results link findings in electrophysiology studies and human fMRI studies and provide evidence that confidence estimates arise from the integration of multiple information processing pathways.
Project description:Drug addiction has been associated with lack of insight into one's own abilities. However, the scope of metacognition impairment among drug users in general and opiate dependent individuals in particular is not fully understood. Investigating the impairments of metacognitive ability in Substance Dependent Individuals (SDIs) in different cognitive tasks could contribute to the ongoing debate over whether metacognition has domain-general or domain-specific neural substrates. We compared metacognitive self-monitoring ability of a group of SDIs during methadone maintenance treatment (n = 23) with a control group (n = 24) in a memory and a visual perceptual task. Post decision self judgements of probability of correct choice were obtained through trial by trial confidence ratings and were used to compute metacognitive ability. Results showed that despite comparable first order performance in the perceptual task, SDIs had lower perceptual metacognition than the control group. However, although SDIs had poorer memory performance, their metacognitive judgements in the memory task were as accurate as the control group. While it is commonly believed that addiction causes pervasive impairment in cognitive functions, including metacognitive ability, we observed that the impairment was only significant in one specific task, the perceptual task, but not in the memory task.
Project description:Established models of perceptual metacognition, the ability to evaluate our perceptual judgements, posit that perceptual confidence depends on the strength or quality of feedforward sensory evidence. However, alternative theoretical accounts suggest the entire perception-action cycle, and not only variation in sensory evidence, is monitored when evaluating confidence in one's percepts. Such models lead to the counterintuitive prediction that perceptual confidence should be directly modulated by features of motor output. To evaluate this proposal here we recorded electromyographic (EMG) activity of motor effectors while subjects performed a near-threshold perceptual discrimination task and reported their confidence in each response in a pre-registered experiment. A subset of trials exhibited subthreshold EMG activity in response effectors before a decision was made. Strikingly, trial-by-trial analysis showed that confidence, but not accuracy, was significantly higher on trials with subthreshold motor activation. These findings support a hypothesis that preparatory motor activity, or a related latent variable, impacts upon confidence over and above performance, consistent with models in which perceptual metacognition integrates information across the perception-action cycle.
Project description:Two fundamental goals of decision making are to select actions that maximize rewards while minimizing costs and to have strong confidence in the accuracy of a judgment. Neural signatures of these two forms of value: the subjective value (SV) of choice alternatives and the value of the judgment (confidence), have both been observed in ventromedial prefrontal cortex (vmPFC). However, the relationship between these dual value signals and their relative time courses are unknown. Twenty-eight men and women underwent fMRI while performing a two-phase approach-avoidance (Ap-Av) task with mixed-outcomes of monetary rewards paired with painful shock stimuli. Neural responses were measured during offer valuation (offer phase) and choice valuation (commit phase) and analyzed with respect to observed decision outcomes, model-estimated SV and confidence. During the offer phase, vmPFC tracked SV and the decision but not confidence. During the commit phase, vmPFC tracked confidence, computed as the quadratic extension of SV, but not the offer valuation nor the decision. In fact, vmPFC responses from the commit phase were selective for confidence even for reject decisions wherein confidence and SV are inversely related. Conversely, activation of the cognitive control network, including within lateral prefrontal cortex (lPFC) and dorsal anterior cingulate cortex (dACC) was associated with ambivalence, during both the offer and commit phases. Taken together, our results reveal complementary representations in vmPFC during value-based decision making that temporally dissociate such that offer valuation (SV) emerges before decision valuation (confidence).
Project description:Anxiety is characterized by low confidence in daily decisions, coupled with high levels of phenomenological stress. Ventromedial prefrontal cortex (vmPFC) plays an integral role in maladaptive anxious behaviors via decreased sensitivity to threatening vs. non-threatening stimuli (fear generalization). vmPFC is also a key node in approach-avoidance decision making requiring two-dimensional integration of rewards and costs. More recently, vmPFC has been implicated as a key cortical input to the sympathetic branch of the autonomic nervous system. However, little is known about the role of this brain region in mediating rapid stress responses elicited by changes in confidence during decision making. We used an approach-avoidance task to examine the relationship between sympathetically mediated cardiac stress responses, vmPFC activity and choice behavior over long and short time-scales. To do this, we collected concurrent fMRI, EKG and impedance cardiography recordings of sympathetic drive while participants made approach-avoidance decisions about monetary rewards paired with painful electric shock stimuli. We observe first that increased sympathetic drive (shorter pre-ejection period) in states lasting minutes are associated with choices involving reduced decision ambivalence. Thus, on this slow time scale, sympathetic drive serves as a proxy for "mobilization" whereby participants are more likely to show consistent value-action mapping. In parallel, imaging analyses reveal that on shorter time scales (estimated with a trial-to-trial GLM), increased vmPFC activity, particularly during low-ambivalence decisions, is associated with decreased sympathetic state. Our findings support a role of sympathetic drive in resolving decision ambivalence across long time horizons and suggest a potential role of vmPFC in modulating this response on a moment-to-moment basis.
Project description:When external feedback about decision outcomes is lacking, agents need to adapt their decision policies based on an internal estimate of the correctness of their choices (i.e., decision confidence). We hypothesized that agents use confidence to continuously update the tradeoff between the speed and accuracy of their decisions: When confidence is low in one decision, the agent needs more evidence before committing to a choice in the next decision, leading to slower but more accurate decisions. We tested this hypothesis by fitting a bounded accumulation decision model to behavioral data from three different perceptual choice tasks. Decision bounds indeed depended on the reported confidence on the previous trial, independent of objective accuracy. This increase in decision bound was predicted by a centro-parietal EEG component sensitive to confidence. We conclude that internally computed neural signals of confidence predict the ongoing adjustment of decision policies.
Project description:It is increasingly clear that simple decisions are made by computing decision values for the options under consideration, and then comparing these values to make a choice. Computational models of this process suggest that it involves the accumulation of information over time, but little is known about the temporal course of valuation in the brain. To examine this, we manipulated the available decision time and observed the consequences in the brain and behavioral correlates of choice. Participants were scanned with functional magnetic resonance imaging while they chose to eat or not eat basic food items, in two conditions differing in the amount of time provided for choice. After identifying valuation-related regions with unbiased whole-brain general linear models, we analyzed two regions of interest: ventromedial prefrontal cortex (VMPFC) and dorsolateral prefrontal cortex (DLPFC). Finite impulse response models of the upsampled estimated neural activity from those regions allowed us to examine the onset, duration and termination of decision value signals, and to compare across regions. We found evidence for the immediate onset of value computation in both regions, but an extended duration with longer decision time. However, this was not accompanied by behavioral changes in either the accuracy or determinants of choice. Finally, there was modest evidence that DLPFC computation correlated with, but lagged behind, VMPFC computation, suggesting the sharing of information across these regions. These findings have important implications for models of decision value computation and choice.
Project description:Decision-making is usually accompanied by metacognition, through which a decision maker monitors uncertainty regarding a decision and may then consequently revise the decision. These metacognitive processes can occur prior to or in the absence of feedback. However, the neural mechanisms of metacognition remain controversial. One theory proposes an independent neural system for metacognition in the prefrontal cortex (PFC); the other, that metacognitive processes coincide and overlap with the systems used for the decision-making process per se. In this study, we devised a novel "decision-redecision" paradigm to investigate the neural metacognitive processes involved in redecision as compared to the initial decision-making process. The participants underwent a perceptual decision-making task and a rule-based decision-making task during functional magnetic resonance imaging (fMRI). We found that the anterior PFC, including the dorsal anterior cingulate cortex (dACC) and lateral frontopolar cortex (lFPC), were more extensively activated after the initial decision. The dACC activity in redecision positively scaled with decision uncertainty and correlated with individual metacognitive uncertainty monitoring abilities-commonly occurring in both tasks-indicating that the dACC was specifically involved in decision uncertainty monitoring. In contrast, the lFPC activity seen in redecision processing was scaled with decision uncertainty reduction and correlated with individual accuracy changes-positively in the rule-based decision-making task and negatively in the perceptual decision-making task. Our results show that the lFPC was specifically involved in metacognitive control of decision adjustment and was subject to different control demands of the tasks. Therefore, our findings support that a separate neural system in the PFC is essentially involved in metacognition and further, that functions of the PFC in metacognition are dissociable.
Project description:Perception and cognition in the brain are naturally characterized as spatiotemporal processes. Decision-making, for example, depends on coordinated patterns of neural activity cascading across the brain, running in time from stimulus to response and in space from primary sensory regions to the frontal lobe. Measuring this cascade is key to developing an understanding of brain function. Here we report on a novel methodology that employs multi-modal imaging for inferring this cascade in humans at unprecedented spatiotemporal resolution. Specifically, we develop an encoding model to link simultaneously measured electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) signals to infer high-resolution spatiotemporal brain dynamics during a perceptual decision. After demonstrating replication of results from the literature, we report previously unobserved sequential reactivation of a substantial fraction of the pre-response network whose magnitude correlates with a proxy for decision confidence. Our encoding model, which temporally tags BOLD activations using time localized EEG variability, identifies a coordinated and spatially distributed neural cascade that is associated with a perceptual decision. In general the methodology illuminates complex brain dynamics that would otherwise be unobservable using fMRI or EEG acquired separately.
Project description:From an early age, individuals with autism spectrum disorder (ASD) spend less time engaged in social interaction compared to typically developing peers (TD). One reason behind this behavior may be that the brains of children diagnosed with ASD do not attribute enough value to potential social exchanges as compared to the brains of typically developing children; thus, potential social exchanges are avoided because other environmental stimuli are more highly valued by default. Neurobiological investigations into the mechanisms underlying value-based decision-making has shown that the ventral medial prefrontal cortex (vmPFC) is critical for encoding the expected outcome value of different actions corresponding to distinct environmental cues. Here, we tested the hypothesis that the responsiveness of the vmPFC in children diagnosed with ASD (compared to TD controls) is diminished for visual cues that represent highly valued social interaction. Using a passive picture viewing task and functional magnetic resonance imaging (fMRI) we measured the response of an a priori defined region of interest in the vmPFC in children diagnosed with ASD and an age-matched TD cohort. We show that the average response of the vmPFC is significantly diminished in the ASD group. Further, we demonstrate that a single-stimulus and less than 30?s of fMRI data are sufficient to differentiate the ASD and TD cohorts. These findings are consistent with the hypothesis that the brains of children with ASD do not encode the value of social exchange in the same manner as TD children. The latter finding suggests the possibility of utilizing single-stimulus fMRI as a potential biologically based diagnostic tool to augment traditional clinical approaches.