Mood and implicit confidence independently fluctuate at different time scales.

Mood is an important ingredient of decision-making. Human beings are immersed into a sea of ​​emotions where episodes of high mood alternate with episodes of low mood. While changes in mood are well characterized, little is known about how these fluctuations interact with metacognition, and in particular with confidence about our decisions. We evaluated how implicit measurements of confidence are related with mood states of human participants through two online longitudinal experiments involving mood self-reports and visual discrimination decision-making tasks. Implicit confidence was assessed on each session by monitoring the proportion of opt-out trials when an opt-out option was available, as well as the median reaction time on standard correct trials as a secondary proxy of confidence. We first report a strong coupling between mood, stress, food enjoyment, and quality of sleep reported by participants in the same session. Second, we confirmed that the proportion of opt-out responses as well as reaction times in non-opt-out trials provided reliable indices of confidence in each session. We introduce a normative measure of overconfidence based on the pattern of opt-out selection and the signal-detection-theory framework. Finally and crucially, we found that mood, sleep quality, food enjoyment, and stress level are not consistently coupled with these implicit confidence markers, but rather they fluctuate at different time scales: mood-related states display faster fluctuations (over one day or half-a-day) than confidence level (two-and-a-half days). Therefore, our findings suggest that spontaneous fluctuations of mood and confidence in decision making are independent in the healthy adult population.

Balance between breadth and depth in human many-alternative decisions.

Many everyday life decisions require allocating finite resources, such as attention or time, to examine multiple available options, like choosing a food supplier online. In cases like these, resources can be spread across many options (breadth) or focused on a few of them (depth). Whilst theoretical work has described how finite resources should be allocated to maximize utility in these problems, evidence about how humans balance breadth and depth is currently lacking. We introduce a novel experimental paradigm where humans make a many-alternative decision under finite resources. In an imaginary scenario, participants allocate a finite budget to sample amongst multiple apricot suppliers in order to estimate the quality of their fruits, and ultimately choose the best one. We found that at low budget capacity participants sample as many suppliers as possible, and thus prefer breadth, whereas at high capacities participants sample just a few chosen alternatives in depth, and intentionally ignore the rest. The number of alternatives sampled increases with capacity following a power law with an exponent close to 3/4. In richer environments, where good outcomes are more likely, humans further favour depth. Participants deviate from optimality and tend to allocate capacity amongst the selected alternatives more homogeneously than it would be optimal, but the impact on the outcome is small. Overall, our results undercover a rich phenomenology of close-to-optimal behaviour and biases in complex choices.

Deep imagination is a close to optimal policy for planning in large decision trees under limited resources.

Many decisions involve choosing an uncertain course of action in deep and wide decision trees, as when we plan to visit an exotic country for vacation. In these cases, exhaustive search for the best sequence of actions is not tractable due to the large number of possibilities and limited time or computational resources available to make the decision. Therefore, planning agents need to balance breadth-considering many actions in the first few tree levels-and depth-considering many levels but few actions in each of them-to allocate optimally their finite search capacity. We provide efficient analytical solutions and numerical analysis to the problem of allocating finite sampling capacity in one shot to infinitely large decision trees, both in the time discounted and undiscounted cases. We find that in general the optimal policy is to allocate few samples per level so that deep levels can be reached, thus favoring depth over breadth search. In contrast, in poor environments and at low capacity, it is best to broadly sample branches at the cost of not sampling deeply, although this policy is marginally better than deep allocations. Our results can provide a theoretical foundation for why human reasoning is pervaded by imagination-based processes.

Optimal Allocation of Finite Sampling Capacity in Accumulator Models of Multialternative Decision Making.

When facing many options, we narrow down our focus to very few of them. Although behaviors like this can be a sign of heuristics, they can actually be optimal under limited cognitive resources. Here, we study the problem of how to optimally allocate limited sampling time to multiple options, modeled as accumulators of noisy evidence, to determine the most profitable one. We show that the effective sampling capacity of an agent increases with both available time and the discriminability of the options, and optimal policies undergo a sharp transition as a function of it. For small capacity, it is best to allocate time evenly to exactly five options and to ignore all the others, regardless of the prior distribution of rewards. For large capacities, the optimal number of sampled accumulators grows sublinearly, closely following a power law as a function of capacity for a wide variety of priors. We find that allocating equal times to the sampled accumulators is better than using uneven time allocations. Our work highlights that multialternative decisions are endowed with breadth-depth tradeoffs, demonstrates how their optimal solutions depend on the amount of limited resources and the variability of the environment, and shows that narrowing down to a handful of options is always optimal for small capacities.

Correction: Representation of foreseeable choice outcomes in orbitofrontal cortex triplet-wise interactions.

[This corrects the article DOI: 10.1371/journal.pcbi.1007862.].

The dynamics of decision-making and action during active sampling.

Embodied Cognition Theories (ECTs) of decision-making propose that the decision process pervades the execution of choice actions and manifests itself in these actions. Decision-making scenarios where actions not only express the choice but also help sample information can provide a valuable, ecologically relevant model for this framework. We present a study to address this paradigmatic situation in humans. Subjects categorized (2AFC task) a central object image, blurred to different extents, by moving a cursor toward the left or right of the display. Upward cursor movements reduced the image blur and could be used to sample information. Thus, actions for decision and actions for sampling were orthogonal to each other. We analyzed response trajectories to test whether information-sampling movements co-occurred with the ongoing decision process. Trajectories were bimodally distributed, with one kind being direct towards one response option (non-sampling), and the other kind containing an initial upward component before veering off towards an option (sampling). This implies that there was an initial decision at the early stage of a trial, whether to sample information or not. Importantly, in sampling trials trajectories were not purely upward, but rather had a significant horizontal deviation early on. This result suggests that movements to sample information exhibit an online interaction with the decision process, therefore supporting the prediction of the ECTs under ecologically relevant constrains.

Sense of agency for mental actions: Insights from a belief-based action-effect paradigm.

A substantial body of research has converged on the idea that the sense of agency arises from the integration of multiple sources of information. In this study, we investigated whether a measurable sense of agency can be detected for mental actions, without the contribution of motor components. We used a fake action-effect paradigm, where participants were led to think that a motor action or a particular thought could trigger a sound. Results showed that the sense of agency, when measured through explicit reports, was of comparable strength for motor and mental actions. The intentional binding effect, a phenomenon typically associated with the experience of agency, was also observed for both motor and mental actions. Taken together, our results provide novel insights into the specific role of intentional cues in instantiating a sense of agency, even in the absence of motor signals.

Computational Modeling of Information Propagation during the Sleep-Waking Cycle.

Non-threatening familiar sounds can go unnoticed during sleep despite the fact that they enter our brain by exciting the auditory nerves. Extracellular cortical recordings in the primary auditory cortex of rodents show that an increase in firing rate in response to pure tones during deep phases of sleep is comparable to those evoked during wakefulness. This result challenges the hypothesis that during sleep cortical responses are weakened through thalamic gating. An alternative explanation comes from the observation that the spatiotemporal spread of the evoked activity by transcranial magnetic stimulation in humans is reduced during non-rapid eye movement (NREM) sleep as compared to the wider propagation to other cortical regions during wakefulness. Thus, cortical responses during NREM sleep remain local and the stimulus only reaches nearby neuronal populations. We aim at understanding how this behavior emerges in the brain as it spontaneously shifts between NREM sleep and wakefulness. To do so, we have used a computational neural-mass model to reproduce the dynamics of the sensory auditory cortex and corresponding local field potentials in these two brain states. Following the synaptic homeostasis hypothesis, an increase in a single parameter, namely the excitatory conductance g¯AMPA, allows us to place the model from NREM sleep into wakefulness. In agreement with the experimental results, the endogenous dynamics during NREM sleep produces a comparable, even higher, response to excitatory inputs to the ones during wakefulness. We have extended the model to two bidirectionally connected cortical columns and have quantified the propagation of an excitatory input as a function of their coupling. We have found that the general increase in all conductances of the cortical excitatory synapses that drive the system from NREM sleep to wakefulness does not boost the effective connectivity between cortical columns. Instead, it is the inter-/intra-conductance ratio of cortical excitatory synapses that should raise to facilitate information propagation across the brain.

Ketamine disrupts naturalistic coding of working memory in primate lateral prefrontal cortex networks.

Ketamine is a dissociative anesthetic drug, which has more recently emerged as a rapid-acting antidepressant. When acutely administered at subanesthetic doses, ketamine causes cognitive deficits like those observed in patients with schizophrenia, including impaired working memory. Although these effects have been linked to ketamine's action as an N-methyl-D-aspartate receptor antagonist, it is unclear how synaptic alterations translate into changes in brain microcircuit function that ultimately influence cognition. Here, we administered ketamine to rhesus monkeys during a spatial working memory task set in a naturalistic virtual environment. Ketamine induced transient working memory deficits while sparing perceptual and motor skills. Working memory deficits were accompanied by decreased responses of fast spiking inhibitory interneurons and increased responses of broad spiking excitatory neurons in the lateral prefrontal cortex. This translated into a decrease in neuronal tuning and information encoded by neuronal populations about remembered locations. Our results demonstrate that ketamine differentially affects neuronal types in the neocortex; thus, it perturbs the excitation inhibition balance within prefrontal microcircuits and ultimately leads to selective working memory deficits.

Prefrontal cortex represents heuristics that shape choice bias and its integration into future behavior.

Goal-directed behavior requires integrating sensory information with prior knowledge about the environment. Behavioral biases that arise from these priors could increase positive outcomes when the priors match the true structure of the environment, but mismatches also happen frequently and could cause unfavorable outcomes. Biases that reduce gains and fail to vanish with training indicate fundamental suboptimalities arising from ingrained heuristics of the brain. Here, we report systematic, gain-reducing choice biases in highly trained monkeys performing a motion direction discrimination task where only the current stimulus is behaviorally relevant. The monkey's bias fluctuated at two distinct time scales: slow, spanning tens to hundreds of trials, and fast, arising from choices and outcomes of the most recent trials. Our findings enabled single trial prediction of biases, which influenced the choice especially on trials with weak stimuli. The pre-stimulus activity of neuronal ensembles in the monkey prearcuate gyrus represented these biases as an offset along the decision axis in the state space. This offset persisted throughout the stimulus viewing period, when sensory information was integrated, leading to a biased choice. The pre-stimulus representation of history-dependent bias was functionally indistinguishable from the neural representation of upcoming choice before stimulus onset, validating our model of single-trial biases and suggesting that pre-stimulus representation of choice could be fully defined by biases inferred from behavioral history. Our results indicate that the prearcuate gyrus reflects intrinsic heuristics that compute bias signals, as well as the mechanisms that integrate them into the oculomotor decision-making process.

Scaling of sensory information in large neural populations shows signatures of information-limiting correlations.

How is information distributed across large neuronal populations within a given brain area? Information may be distributed roughly evenly across neuronal populations, so that total information scales linearly with the number of recorded neurons. Alternatively, the neural code might be highly redundant, meaning that total information saturates. Here we investigate how sensory information about the direction of a moving visual stimulus is distributed across hundreds of simultaneously recorded neurons in mouse primary visual cortex. We show that information scales sublinearly due to correlated noise in these populations. We compartmentalized noise correlations into information-limiting and nonlimiting components, then extrapolate to predict how information grows with even larger neural populations. We predict that tens of thousands of neurons encode 95% of the information about visual stimulus direction, much less than the number of neurons in primary visual cortex. These findings suggest that the brain uses a widely distributed, but nonetheless redundant code that supports recovering most sensory information from smaller subpopulations.

The covariance perceptron: A new paradigm for classification and processing of time series in recurrent neuronal networks.

Learning in neuronal networks has developed in many directions, in particular to reproduce cognitive tasks like image recognition and speech processing. Implementations have been inspired by stereotypical neuronal responses like tuning curves in the visual system, where, for example, ON/OFF cells fire or not depending on the contrast in their receptive fields. Classical models of neuronal networks therefore map a set of input signals to a set of activity levels in the output of the network. Each category of inputs is thereby predominantly characterized by its mean. In the case of time series, fluctuations around this mean constitute noise in this view. For this paradigm, the high variability exhibited by the cortical activity may thus imply limitations or constraints, which have been discussed for many years. For example, the need for averaging neuronal activity over long periods or large groups of cells to assess a robust mean and to diminish the effect of noise correlations. To reconcile robust computations with variable neuronal activity, we here propose a conceptual change of perspective by employing variability of activity as the basis for stimulus-related information to be learned by neurons, rather than merely being the noise that corrupts the mean signal. In this new paradigm both afferent and recurrent weights in a network are tuned to shape the input-output mapping for covariances, the second-order statistics of the fluctuating activity. When including time lags, covariance patterns define a natural metric for time series that capture their propagating nature. We develop the theory for classification of time series based on their spatio-temporal covariances, which reflect dynamical properties. We demonstrate that recurrent connectivity is able to transform information contained in the temporal structure of the signal into spatial covariances. Finally, we use the MNIST database to show how the covariance perceptron can capture specific second-order statistical patterns generated by moving digits.

Heuristics and optimal solutions to the breadth-depth dilemma.

In multialternative risky choice, we are often faced with the opportunity to allocate our limited information-gathering capacity between several options before receiving feedback. In such cases, we face a natural trade-off between breadth-spreading our capacity across many options-and depth-gaining more information about a smaller number of options. Despite its broad relevance to daily life, including in many naturalistic foraging situations, the optimal strategy in the breadth-depth trade-off has not been delineated. Here, we formalize the breadth-depth dilemma through a finite-sample capacity model. We find that, if capacity is small (∼10 samples), it is optimal to draw one sample per alternative, favoring breadth. However, for larger capacities, a sharp transition is observed, and it becomes best to deeply sample a very small fraction of alternatives, which roughly decreases with the square root of capacity. Thus, ignoring most options, even when capacity is large enough to shallowly sample all of them, is a signature of optimal behavior. Our results also provide a rich casuistic for metareasoning in multialternative decisions with bounded capacity using close-to-optimal heuristics.

Representation of foreseeable choice outcomes in orbitofrontal cortex triplet-wise interactions.

Shared neuronal variability has been shown to modulate cognitive processing. However, the relationship between shared variability and behavioral performance is heterogeneous and complex in frontal areas such as the orbitofrontal cortex (OFC). Mounting evidence shows that single-units in OFC encode a detailed cognitive map of task-space events, but the existence of a robust neuronal ensemble coding for the predictability of choice outcome is less established. Here, we hypothesize that the coding of foreseeable outcomes is potentially unclear from the analysis of units activity and their pairwise correlations. However, this code might be established more conclusively when higher-order neuronal interactions are mapped to the choice outcome. As a case study, we investigated the trial-to-trial shared variability of neuronal ensemble activity during a two-choice interval-discrimination task in rodent OFC, specifically designed such that a lose-switch strategy is optimal by repeating the rewarded stimulus in the upcoming trial. Results show that correlations among triplets are higher during correct choices with respect to incorrect ones, and that this is sustained during the entire trial. This effect is not observed for pairwise nor for higher than third-order correlations. This scenario is compatible with constellations of up to three interacting units assembled during trials in which the task is performed correctly. More interestingly, a state-space spanned by such constellations shows that only correct outcome states that can be successfully predicted are robust over 100 trials of the task, and thus they can be accurately decoded. However, both incorrect and unpredictable outcome representations were unstable and thus non-decodeable, due to spurious negative correlations. Our results suggest that predictability of successful outcomes, and hence the optimal behavioral strategy, can be mapped out in OFC ensemble states reliable over trials of the task, and revealed by sufficiency complex neuronal interactions.

A roadmap to integrate astrocytes into Systems Neuroscience.

Systems neuroscience is still mainly a neuronal field, despite the plethora of evidence supporting the fact that astrocytes modulate local neural circuits, networks, and complex behaviors. In this article, we sought to identify which types of studies are necessary to establish whether astrocytes, beyond their well-documented homeostatic and metabolic functions, perform computations implementing mathematical algorithms that sub-serve coding and higher-brain functions. First, we reviewed Systems-like studies that include astrocytes in order to identify computational operations that these cells may perform, using Ca2+ transients as their encoding language. The analysis suggests that astrocytes may carry out canonical computations in a time scale of subseconds to seconds in sensory processing, neuromodulation, brain state, memory formation, fear, and complex homeostatic reflexes. Next, we propose a list of actions to gain insight into the outstanding question of which variables are encoded by such computations. The application of statistical analyses based on machine learning, such as dimensionality reduction and decoding in the context of complex behaviors, combined with connectomics of astrocyte-neuronal circuits, is, in our view, fundamental undertakings. We also discuss technical and analytical approaches to study neuronal and astrocytic populations simultaneously, and the inclusion of astrocytes in advanced modeling of neural circuits, as well as in theories currently under exploration such as predictive coding and energy-efficient coding. Clarifying the relationship between astrocytic Ca2+ and brain coding may represent a leap forward toward novel approaches in the study of astrocytes in health and disease.

The Effects of Population Tuning and Trial-by-Trial Variability on Information Encoding and Behavior.

Identifying the features of population responses that are relevant to the amount of information encoded by neuronal populations is a crucial step toward understanding population coding. Statistical features, such as tuning properties, individual and shared response variability, and global activity modulations, could all affect the amount of information encoded and modulate behavioral performance. We show that two features in particular affect information: the modulation of population responses across conditions (population signal) and the inverse population covariability along the modulation axis (projected precision). We demonstrate that fluctuations of these two quantities are correlated with fluctuations of behavioral performance in various tasks and brain regions consistently across 4 monkeys (1 female and 1 male Macaca mulatta; and 2 male Macaca fascicularis). In contrast, fluctuations in mean correlations among neurons and global activity have negligible or inconsistent effects on the amount of information encoded and behavioral performance. We also show that differential correlations reduce the amount of information encoded in finite populations by reducing projected precision. Our results are consistent with predictions of a model that optimally decodes population responses to produce behavior.SIGNIFICANCE STATEMENT The last two or three decades of research have seen hot debates about what features of population tuning and trial-by-trial variability influence the information carried by a population of neurons, with some camps arguing, for instance, that mean pairwise correlations or global fluctuations are important while other camps report opposite results. In this study, we identify the most important features of neural population responses that determine the amount of encoded information and behavioral performance by combining analytic calculations with a novel nonparametric method that allows us to isolate the effects of different statistical features. We tested our hypothesis on 4 macaques, three decision-making tasks, and two brain areas. The predictions of our theory were in agreement with the experimental data.

Human confidence judgments reflect reliability-based hierarchical integration of contextual information.

Our immediate observations must be supplemented with contextual information to resolve ambiguities. However, the context is often ambiguous too, and thus it should be inferred itself to guide behavior. Here, we introduce a novel hierarchical task (airplane task) in which participants should infer a higher-level, contextual variable to inform probabilistic inference about a hidden dependent variable at a lower level. By controlling the reliability of past sensory evidence through varying the sample size of the observations, we find that humans estimate the reliability of the context and combine it with current sensory uncertainty to inform their confidence reports. Behavior closely follows inference by probabilistic message passing between latent variables across hierarchical state representations. Commonly reported inferential fallacies, such as sample size insensitivity, are not present, and neither did participants appear to rely on simple heuristics. Our results reveal uncertainty-sensitive integration of information at different hierarchical levels and temporal scales.

Family of closed-form solutions for two-dimensional correlated diffusion processes.

Diffusion processes with boundaries are models of transport phenomena with wide applicability across many fields. These processes are described by their probability density functions (PDFs), which often obey Fokker-Planck equations (FPEs). While obtaining analytical solutions is often possible in the absence of boundaries, obtaining closed-form solutions to the FPE is more challenging once absorbing boundaries are present. As a result, analyses of these processes have largely relied on approximations or direct simulations. In this paper, we studied two-dimensional, time-homogeneous, spatially correlated diffusion with linear, axis-aligned, absorbing boundaries. Our main result is the explicit construction of a full family of closed-form solutions for their PDFs using the method of images. We found that such solutions can be built if and only if the correlation coefficient ρ between the two diffusing processes takes one of a numerable set of values. Using a geometric argument, we derived the complete set of ρ's where such solutions can be found. Solvable ρ's are given by ρ=-cos(π/k), where k∈Z^{+}∪{+∞}. Solutions were validated in simulations. Qualitative behaviors of the process appear to vary smoothly over ρ, allowing extrapolation from our solutions to cases with unsolvable ρ's.

Instance-based generalization for human judgments about uncertainty.

While previous studies have shown that human behavior adjusts in response to uncertainty, it is still not well understood how uncertainty is estimated and represented. As probability distributions are high dimensional objects, only constrained families of distributions with a low number of parameters can be specified from finite data. However, it is unknown what the structural assumptions are that the brain uses to estimate them. We introduce a novel paradigm that requires human participants of either sex to explicitly estimate the dispersion of a distribution over future observations. Judgments are based on a very small sample from a centered, normally distributed random variable that was suggested by the framing of the task. This probability density estimation task could optimally be solved by inferring the dispersion parameter of a normal distribution. We find that although behavior closely tracks uncertainty on a trial-by-trial basis and resists an explanation with simple heuristics, it is hardly consistent with parametric inference of a normal distribution. Despite the transparency of the simple generating process, participants estimate a distribution biased towards the observed instances while still strongly generalizing beyond the sample. The inferred internal distributions can be well approximated by a nonparametric mixture of spatially extended basis distributions. Thus, our results suggest that fluctuations have an excessive effect on human uncertainty judgments because of representations that can adapt overly flexibly to the sample. This might be of greater utility in more general conditions in structurally uncertain environments.