Threat Expectation Does Not Improve Perceptual Discrimination despite Causing Heightened Priority Processing in the Frontoparietal Network.

Threat cues have been widely shown to elicit increased sensory and attentional neural processing. However, whether this enhanced recruitment leads to measurable behavioral improvements in perception is still in question. Here, we adjudicate between two opposing theories: that threat cues do or do not enhance perceptual sensitivity. We created threat stimuli by pairing one direction of motion in a random dot kinematogram with an aversive sound. While in the MRI scanner, 46 subjects (both men and women) completed a cued (threat/safe/neutral) perceptual decision-making task where they indicated the perceived motion direction of each moving dot stimulus. We found strong evidence that threat cues did not increase perceptual sensitivity compared with safe and neutral cues. This lack of improvement in perceptual decision-making ability occurred despite the threat cue resulting in widespread increases in frontoparietal BOLD activity, as well as increased connectivity between the right insula and the frontoparietal network. These results call into question the intuitive claim that expectation automatically enhances our perception of threat and highlight the role of the frontoparietal network in prioritizing the processing of threat-related environmental cues.

Task learning is subserved by a domain-general brain network.

One of the most important human faculties is the ability to acquire not just new memories but the capacity to perform entirely new tasks. However, little is known about the brain mechanisms underlying the learning of novel tasks. Specifically, it is unclear to what extent learning of different tasks depends on domain-general and/or domain-specific brain mechanisms. Here human subjects (n = 45) learned to perform 6 new tasks while undergoing functional MRI. The different tasks required the engagement of perceptual, motor, and various cognitive processes related to attention, expectation, speed-accuracy tradeoff, and metacognition. We found that a bilateral frontoparietal network was more active during the initial compared with the later stages of task learning, and that this effect was stronger for task variants requiring more new learning. Critically, the same frontoparietal network was engaged by all 6 tasks, demonstrating its domain generality. Finally, although task learning decreased the overall activity in the frontoparietal network, it increased the connectivity strength between the different nodes of that network. These results demonstrate the existence of a domain-general brain network whose activity and connectivity reflect learning for a variety of new tasks, and thus may underlie the human capacity for acquiring new abilities.

Quantifying the contribution of subject and group factors in brain activation.

Research in neuroscience often assumes universal neural mechanisms, but increasing evidence points toward sizeable individual differences in brain activations. What remains unclear is the extent of the idiosyncrasy and whether different types of analyses are associated with different levels of idiosyncrasy. Here we develop a new method for addressing these questions. The method consists of computing the within-subject reliability and subject-to-group similarity of brain activations and submitting these values to a computational model that quantifies the relative strength of group- and subject-level factors. We apply this method to a perceptual decision-making task (n = 50) and find that activations related to task, reaction time, and confidence are influenced equally strongly by group- and subject-level factors. Both group- and subject-level factors are dwarfed by a noise factor, though higher levels of smoothing increases their contributions relative to noise. Overall, our method allows for the quantification of group- and subject-level factors of brain activations and thus provides a more detailed understanding of the idiosyncrasy levels in brain activations.

Confidence response times: Challenging postdecisional models of confidence.

Even though the nature of confidence computations has been the topic of intense interest, little attention has been paid to what confidence response times (cRTs) reveal about the underlying confidence computations. Several previous studies found cRTs to be negatively correlated with confidence in the group as a whole and consequently hypothesized the existence of an intrinsic relationship of cRT with confidence for all subjects. This hypothesis was further used to support postdecisional models of confidence that predict that cRT and confidence should always be negatively correlated. Here we test the alternative hypothesis that cRT is driven by the frequency of confidence responses such that the most frequent confidence ratings are inherently made faster regardless of whether they are high or low. We examined cRTs in three large data sets from the Confidence Database and found that the lowest cRTs occurred for the most frequent confidence rating. In other words, subjects who gave high confidence ratings most frequently had negative confidence-cRT relationships, whereas subjects who gave low confidence ratings most frequently had positive confidence-cRT relationships. In addition, we found a strong across-subject correlation between response time and cRT, suggesting that response speed for both the decision and the confidence rating is influenced by a common factor. Our results show that cRT is not intrinsically linked to confidence and strongly challenge several postdecisional models of confidence.

Stimulation along the anterior-posterior axis of lateral frontal cortex reduces visual serial dependence.

Serial dependence is an attractive pull that recent perceptual history exerts on current judgments. Theory suggests that this bias is due to a form of short-term plasticity prevalent specifically in the frontal lobe. We sought to test the importance of the frontal lobe to serial dependence by disrupting neural activity along its lateral surface during two tasks with distinct perceptual and motor demands. In our first experiment, stimulation of the lateral prefrontal cortex (LPFC) during an oculomotor delayed response task decreased serial dependence only in the first saccade to the target, whereas stimulation posterior to the LPFC decreased serial dependence only in adjustments to eye position after the first saccade. In our second experiment, which used an orientation discrimination task, stimulation anterior to, in, and posterior to the LPFC all caused equivalent decreases in serial dependence. In this experiment, serial dependence occurred only between stimuli at the same location; an alternation bias was observed across hemifields. Frontal stimulation had no effect on the alternation bias. Transcranial magnetic stimulation to parietal cortex had no effect on serial dependence in either experiment. In summary, our experiments provide evidence for both functional differentiation (Experiment 1) and redundancy (Experiment 2) in frontal cortex with respect to serial dependence.

The Impact of Feedback on Perceptual Decision-Making and Metacognition: Reduction in Bias but No Change in Sensitivity.

It is widely believed that feedback improves behavior, but the mechanisms behind this improvement remain unclear. Different theories postulate that feedback has either a direct effect on performance through automatic reinforcement mechanisms or only an indirect effect mediated by a deliberate change in strategy. To adjudicate between these competing accounts, we performed two large experiments on human adults (total N = 518); approximately half the participants received trial-by-trial feedback on a perceptual task, whereas the other half did not receive any feedback. We found that feedback had no effect on either perceptual or metacognitive sensitivity even after 7 days of training. On the other hand, feedback significantly affected participants' response strategies by reducing response bias and improving confidence calibration. These results suggest that the beneficial effects of feedback stem from allowing people to adjust their strategies for performing the task and not from direct reinforcement mechanisms, at least in the domain of perception.

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.

Response Bias Reflects Individual Differences in Sensory Encoding.

Humans exhibit substantial biases in their decision making even in simple two-choice tasks, but the origin of these biases remains unclear. I hypothesized that one source of bias could be individual differences in sensory encoding. Specifically, if one stimulus category gives rise to an internal-evidence distribution with higher variability, then responses should optimally be biased against that stimulus category. Therefore, response bias may reflect a previously unappreciated subject-to-subject difference in the variance of the internal-evidence distributions. I tested this possibility by analyzing data from three different two-choice tasks (ns = 443, 443, and 498). For all three tasks, response bias moved in the direction of the optimal criterion determined by each subject's idiosyncratic internal-evidence variability. These results demonstrate that seemingly random variations in response bias can be driven by individual differences in sensory encoding and are thus partly explained by normative strategies.

Examining the robustness of the relationship between metacognitive efficiency and metacognitive bias.

We recently found a positive relationship between estimates of metacognitive efficiency and metacognitive bias. However, this relationship was only examined on a within-subject level and required binarizing the confidence scale, a technique that introduces methodological difficulties. Here we examined the robustness of the positive relationship between estimates of metacognitive efficiency and metacognitive bias by conducting two different types of analyses. First, we developed a new within-subject analysis technique where the original n-point confidence scale is transformed into two different (n-1)-point scales in a way that mimics a naturalistic change in confidence. Second, we examined the across-subject correlation between metacognitive efficiency and metacognitive bias. Importantly, for both types of analyses, we not only established the direction of the effect but also computed effect sizes. We applied both techniques to the data from three tasks from the Confidence Database (N > 400 in each). We found that both approaches revealed a small to medium positive relationship between metacognitive efficiency and metacognitive bias. These results demonstrate that the positive relationship between metacognitive efficiency and metacognitive bias is robust across several analysis techniques and datasets, and have important implications for future research.

Resource-rational analysis versus resource-rational humans.

Lieder and Griffiths advocate for resource-rational analysis as a methodological device employed by the experimenter. However, at times this methodological device appears to morph into the substantive claim that humans are actually resource-rational. Such morphing is problematic; the methodological approach used by the experimenter and claims about the nature of human behavior ought to be kept completely separate.

Distinguishing the Roles of Dorsolateral and Anterior PFC in Visual Metacognition.

Visual metacognition depends on regions within the prefrontal cortex (PFC). Two areas in particular have been implicated repeatedly: the dorsolateral PFC (DLPFC) and the anterior PFC (aPFC). However, it is still unclear what the function of each of these areas is and how they differ from each other. To establish the specific roles of DLPFC and aPFC in metacognition, we used online transcranial magnetic stimulation (TMS) to interfere causally with their functioning during confidence generation. Human subjects from both sexes performed a perceptual decision making and provided confidence ratings. We found a clear dissociation between the two areas: DLPFC TMS lowered confidence ratings, whereas aPFC TMS increased metacognitive ability, but only for the second half of the experimental blocks. These results support a functional architecture in which DLPFC reads out the strength of the sensory evidence and relays it to aPFC, which makes the confidence judgment by potentially incorporating additional, nonperceptual information. Indeed, simulations from a model that incorporates these putative DLPFC and aPFC functions reproduced our behavioral results. These findings establish DLPFC and aPFC as distinct nodes in a metacognitive network and suggest specific contributions from each of these regions to confidence generation.SIGNIFICANCE STATEMENT The prefrontal cortex (PFC) is known to be critical for metacognition. Two of its subregions, the dorsolateral PFC (DLPFC) and the anterior PFC (aPFC), have been specifically implicated in confidence generation. However, it is unclear whether these regions have distinct functions related to the underlying metacognitive computation. Using a causal intervention with transcranial magnetic stimulation, we demonstrate that DLPFC and aPFC have dissociable contributions: targeting DLPFC decreased average confidence ratings, whereas targeting aPFC affected metacognitive scores specifically. Based on these results, we postulated specific functions for DLPFC and aPFC in metacognitive computation and corroborated them using a computational model that reproduced our results. Our causal results reveal the existence of a specialized modular organization in PFC for confidence generation.

Feature-Specific Awake Reactivation in Human V1 after Visual Training.

Brain activity patterns exhibited during task performance have been shown to spontaneously reemerge in the following restful awake state. Such "awake reactivation" has been observed across higher-order cortex for complex images or associations. However, it is still unclear whether the reactivation extends to primary sensory areas that encode simple stimulus features. To address this question, we trained human subjects from both sexes on a particular visual feature (Gabor orientation) and tested whether this feature will be reactivated immediately after training. We found robust reactivation in human V1 that lasted for at least 8 min after training offset. This effect was not present in higher retinotopic areas, such as V2, V3, V3A, or V4v. Further analyses suggested that the amount of awake reactivation was related to the amount of performance improvement on the visual task. These results demonstrate that awake reactivation extends beyond higher-order areas and also occurs in early sensory cortex.SIGNIFICANCE STATEMENT How do we acquire new memories and skills? New information is known to be consolidated during offline periods of rest. Recent studies suggest that a critical process during this period of consolidation is the spontaneous reactivation of previously experienced patterns of neural activity. However, research in humans has mostly examined such reactivation processes in higher-order cortex. Here we show that awake reactivation occurs even in the primary visual cortex V1 and that this reactivation is related to the amount of behavioral learning. These results pinpoint awake reactivation as a process that likely occurs across the entire human brain and could play an integral role in memory consolidation.

Causal evidence for frontal cortex organization for perceptual decision making.

Although recent research has shown that the frontal cortex has a critical role in perceptual decision making, an overarching theory of frontal functional organization for perception has yet to emerge. Perceptual decision making is temporally organized such that it requires the processes of selection, criterion setting, and evaluation. We hypothesized that exploring this temporal structure would reveal a large-scale frontal organization for perception. A causal intervention with transcranial magnetic stimulation revealed clear specialization along the rostrocaudal axis such that the control of successive stages of perceptual decision making was selectively affected by perturbation of successively rostral areas. Simulations with a dynamic model of decision making suggested distinct computational contributions of each region. Finally, the emergent frontal gradient was further corroborated by functional MRI. These causal results provide an organizational principle for the role of frontal cortex in the control of perceptual decision making and suggest specific mechanistic contributions for its different subregions.

Resolving Age-Related Differences in Working Memory: Equating Perception and Attention Makes Older Adults Remember as Well as Younger Adults.

OBJECTIVES: Older adults show clear deficits in working memory functioning. Here, we investigate the often-reported decline in focus switching, that is, the ability to shift items from the focus of attention into working memory, and back. Specifically, we examined whether equating subjects on early processing (perception and attention) might ameliorate the deficit. METHOD: We examined 1-Back and 2-Back performance in younger and older adults, with line segments of different orientation as the stimuli. Stimuli were calibrated depending on each individual's 75% threshold for 1-Back performance. Subjects made match/mismatch judgments. RESULTS: After the calibration on 1-Back performance, no age-related differences were found on either accuracy or sensitivity in the 2-Back task. Additionally, when investigating focus-switch trials versus non-focus-switch trials in a random-order 2-Back task, older adults were more efficient at switching the focus of attention than younger adults. DISCUSSION: These results provide evidence for the view that age-related limitations in focus switching in working memory are caused (at least in part) by changes in early processing (perception and attention), suggesting that (at least some of the) age-related differences in working memory functioning may be due to shifts in trade-off between early processing and memory-related processing.

The Bayesian brain: What is it and do humans have it?

It has been widely asserted that humans have a "Bayesian brain." Surprisingly, however, this term has never been defined and appears to be used differently by different authors. I argue that Bayesian brain should be used to denote the realist view that brains are actual Bayesian machines and point out that there is currently no evidence for such a claim.

Behavior is sensible but not globally optimal: Seeking common ground in the optimality debate.

The disagreements among commentators may appear substantial, but much of the debate seems to stem from inconsistent use of the term optimality. Optimality can be used to indicate sensible behavior (adapted to the environment), globally optimal behavior (fully predicted from optimality considerations alone), locally optimal behavior (conforming to a specific model), and optimality as an empirical strategy (a tool for studying behavior). Distinguishing among these different concepts uncovers considerable common ground in the optimality debate.

Suboptimality in perceptual decision making.

Human perceptual decisions are often described as optimal. Critics of this view have argued that claims of optimality are overly flexible and lack explanatory power. Meanwhile, advocates for optimality have countered that such criticisms single out a few selected papers. To elucidate the issue of optimality in perceptual decision making, we review the extensive literature on suboptimal performance in perceptual tasks. We discuss eight different classes of suboptimal perceptual decisions, including improper placement, maintenance, and adjustment of perceptual criteria; inadequate tradeoff between speed and accuracy; inappropriate confidence ratings; misweightings in cue combination; and findings related to various perceptual illusions and biases. In addition, we discuss conceptual shortcomings of a focus on optimality, such as definitional difficulties and the limited value of optimality claims in and of themselves. We therefore advocate that the field drop its emphasis on whether observed behavior is optimal and instead concentrate on building and testing detailed observer models that explain behavior across a wide range of tasks. To facilitate this transition, we compile the proposed hypotheses regarding the origins of suboptimal perceptual decisions reviewed here. We argue that verifying, rejecting, and expanding these explanations for suboptimal behavior - rather than assessing optimality per se - should be among the major goals of the science of perceptual decision making.

Confidence Leak in Perceptual Decision Making.

People live in a continuous environment in which the visual scene changes on a slow timescale. It has been shown that to exploit such environmental stability, the brain creates a continuity field in which objects seen seconds ago influence the perception of current objects. What is unknown is whether a similar mechanism exists at the level of metacognitive representations. In three experiments, we demonstrated a robust intertask confidence leak-that is, confidence in one's response on a given task or trial influencing confidence on the following task or trial. This confidence leak could not be explained by response priming or attentional fluctuations. Better ability to modulate confidence leak predicted higher capacity for metacognition as well as greater gray matter volume in the prefrontal cortex. A model based on normative principles from Bayesian inference explained the results by postulating that observers subjectively estimate the perceptual signal strength in a stable environment. These results point to the existence of a novel metacognitive mechanism mediated by regions in the prefrontal cortex.

Prestimulus oscillatory activity over motor cortex reflects perceptual expectations.

When perceptual decisions are coupled to a specific effector, preparatory motor cortical activity may provide a window into the dynamics of the perceptual choice. Specifically, previous studies have observed a buildup of choice-selective activity in motor regions over time reflecting the integrated sensory evidence provided by visual cortex. Here we ask how this choice-selective motor activity is modified by prior expectation during a visual motion discrimination task. Computational models of decision making formalize decisions as the accumulation of evidence from a starting point to a decision bound. Within this framework, expectation could change the starting point, rate of accumulation, or the decision bound. Using magneto-encephalography in human observers, we specifically tested for changes in the starting point in choice-selective oscillatory activity over motor cortex. Inducing prior expectation about motion direction biased subjects' perceptual judgments as well as the choice-selective motor activity in the 8-30 Hz frequency range before stimulus onset; the individual strength of these behavioral and neural biases were correlated across subjects. In the absence of explicit expectation cues, spontaneous biases in choice-selective activity were evident over motor cortex. These also predicted eventual perceptual choice and were, at least in part, induced by the choice on the previous trial. We conclude that both endogenous and explicitly induced perceptual expectations bias the starting point of decision-related activity, before the accumulation of sensory evidence.

How do humans give confidence? A comprehensive comparison of process models of perceptual metacognition.

Humans have the metacognitive ability to assess the accuracy of their decisions via confidence judgments. Several computational models of confidence have been developed but not enough has been done to compare these models, making it difficult to adjudicate between them. Here, we compare 14 popular models of confidence that make various assumptions, such as confidence being derived from postdecisional evidence, from positive (decision-congruent) evidence, from posterior probability computations, or from a separate decision-making system for metacognitive judgments. We fit all models to three large experiments in which subjects completed a basic perceptual task with confidence ratings. In Experiments 1 and 2, the best-fitting model was the lognormal meta noise (LogN) model, which postulates that confidence is selectively corrupted by signal-dependent noise. However, in Experiment 3, the positive evidence (PE) model provided the best fits. We evaluated a new model combining the two consistently best-performing models-LogN and the weighted evidence and visibility (WEV). The resulting model, which we call logWEV, outperformed its individual counterparts and the PE model across all data sets, offering a better, more generalizable explanation for these data. Parameter and model recovery analyses showed mostly good recoverability but with important exceptions carrying implications for our ability to discriminate between models. Finally, we evaluated each model's ability to explain different patterns in the data, which led to additional insight into their performances. These results comprehensively characterize the relative adequacy of current confidence models to fit data from basic perceptual tasks and highlight the most plausible mechanisms underlying confidence generation. (PsycInfo Database Record (c) 2024 APA, all rights reserved).