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.

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.

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.

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

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

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.

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.

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.

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.

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.

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.

Estimation of Directed Effective Connectivity from fMRI Functional Connectivity Hints at Asymmetries of Cortical Connectome.

The brain exhibits complex spatio-temporal patterns of activity. This phenomenon is governed by an interplay between the internal neural dynamics of cortical areas and their connectivity. Uncovering this complex relationship has raised much interest, both for theory and the interpretation of experimental data (e.g., fMRI recordings) using dynamical models. Here we focus on the so-called inverse problem: the inference of network parameters in a cortical model to reproduce empirically observed activity. Although it has received a lot of interest, recovering directed connectivity for large networks has been rather unsuccessful so far. The present study specifically addresses this point for a noise-diffusion network model. We develop a Lyapunov optimization that iteratively tunes the network connectivity in order to reproduce second-order moments of the node activity, or functional connectivity. We show theoretically and numerically that the use of covariances with both zero and non-zero time shifts is the key to infer directed connectivity. The first main theoretical finding is that an accurate estimation of the underlying network connectivity requires that the time shift for covariances is matched with the time constant of the dynamical system. In addition to the network connectivity, we also adjust the intrinsic noise received by each network node. The framework is applied to experimental fMRI data recorded for subjects at rest. Diffusion-weighted MRI data provide an estimate of anatomical connections, which is incorporated to constrain the cortical model. The empirical covariance structure is reproduced faithfully, especially its temporal component (i.e., time-shifted covariances) in addition to the spatial component that is usually the focus of studies. We find that the cortical interactions, referred to as effective connectivity, in the tuned model are not reciprocal. In particular, hubs are either receptors or feeders: they do not exhibit both strong incoming and outgoing connections. Our results sets a quantitative ground to explore the propagation of activity in the cortex.

Poisson-like spiking in circuits with probabilistic synapses.

Neuronal activity in cortex is variable both spontaneously and during stimulation, and it has the remarkable property that it is Poisson-like over broad ranges of firing rates covering from virtually zero to hundreds of spikes per second. The mechanisms underlying cortical-like spiking variability over such a broad continuum of rates are currently unknown. We show that neuronal networks endowed with probabilistic synaptic transmission, a well-documented source of variability in cortex, robustly generate Poisson-like variability over several orders of magnitude in their firing rate without fine-tuning of the network parameters. Other sources of variability, such as random synaptic delays or spike generation jittering, do not lead to Poisson-like variability at high rates because they cannot be sufficiently amplified by recurrent neuronal networks. We also show that probabilistic synapses predict Fano factor constancy of synaptic conductances. Our results suggest that synaptic noise is a robust and sufficient mechanism for the type of variability found in cortex.

Bayesian sampling in visual perception.

It is well-established that some aspects of perception and action can be understood as probabilistic inferences over underlying probability distributions. In some situations, it would be advantageous for the nervous system to sample interpretations from a probability distribution rather than commit to a particular interpretation. In this study, we asked whether visual percepts correspond to samples from the probability distribution over image interpretations, a form of sampling that we refer to as Bayesian sampling. To test this idea, we manipulated pairs of sensory cues in a bistable display consisting of two superimposed moving drifting gratings, and we asked subjects to report their perceived changes in depth ordering. We report that the fractions of dominance of each percept follow the multiplicative rule predicted by Bayesian sampling. Furthermore, we show that attractor neural networks can sample probability distributions if input currents add linearly and encode probability distributions with probabilistic population codes.

Complex behavior from intrinsic motivation to occupy future action-state path space.

Most theories of behavior posit that agents tend to maximize some form of reward or utility. However, animals very often move with curiosity and seem to be motivated in a reward-free manner. Here we abandon the idea of reward maximization and propose that the goal of behavior is maximizing occupancy of future paths of actions and states. According to this maximum occupancy principle, rewards are the means to occupy path space, not the goal per se; goal-directedness simply emerges as rational ways of searching for resources so that movement, understood amply, never ends. We find that action-state path entropy is the only measure consistent with additivity and other intuitive properties of expected future action-state path occupancy. We provide analytical expressions that relate the optimal policy and state-value function and prove convergence of our value iteration algorithm. Using discrete and continuous state tasks, including a high-dimensional controller, we show that complex behaviors such as "dancing", hide-and-seek, and a basic form of altruistic behavior naturally result from the intrinsic motivation to occupy path space. All in all, we present a theory of behavior that generates both variability and goal-directedness in the absence of reward maximization.

Gaze-centered gating, reactivation, and reevaluation of economic value in orbitofrontal cortex.

During economic choice, options are often considered in alternation, until commitment. Nonetheless, neuroeconomics typically ignores the dynamic aspects of deliberation. We trained two male macaques to perform a value-based decision-making task in which two risky offers were presented in sequence at the opposite sides of the visual field, each followed by a delay epoch where offers were invisible. Surprisingly, during the two delays, subjects tend to look at empty locations where the offers had previously appeared, with longer fixations increasing the probability of choosing the associated offer. Spiking activity in orbitofrontal cortex reflects the value of the gazed offer, or of the offer associated with the gazed empty spatial location, even if it is not the most recent. This reactivation reflects a reevaluation process, as fluctuations in neural spiking correlate with upcoming choice. Our results suggest that look-at-nothing gazing triggers the reactivation of a previously seen offer for further evaluation.

The cost of accumulating evidence in perceptual decision making.

Decision making often involves the accumulation of information over time, but acquiring information typically comes at a cost. Little is known about the cost incurred by animals and humans for acquiring additional information from sensory variables due, for instance, to attentional efforts. Through a novel integration of diffusion models and dynamic programming, we were able to estimate the cost of making additional observations per unit of time from two monkeys and six humans in a reaction time (RT) random-dot motion discrimination task. Surprisingly, we find that the cost is neither zero nor constant over time, but for the animals and humans features a brief period in which it is constant but increases thereafter. In addition, we show that our theory accurately matches the observed reaction time distributions for each stimulus condition, the time-dependent choice accuracy both conditional on stimulus strength and independent of it, and choice accuracy and mean reaction times as a function of stimulus strength. The theory also correctly predicts that urgency signals in the brain should be independent of the difficulty, or stimulus strength, at each trial.

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.

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.

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.