The parieto-occipital cortex is a candidate neural substrate for the human ability to approximate Bayesian inference.

Adaptive decision-making often requires one to infer unobservable states based on incomplete information. Bayesian logic prescribes that individuals should do so by estimating the posterior probability by integrating the prior probability with new information, but the neural basis of this integration is incompletely understood. We record fMRI during a task in which participants infer the posterior probability of a hidden state while we independently modulate the prior probability and likelihood of evidence regarding the state; the task incentivizes participants to make accurate inferences and dissociates expected value from posterior probability. Here we show that activation in a region of left parieto-occipital cortex independently tracks the subjective posterior probability, combining its subcomponents of prior probability and evidence likelihood, and reflecting the individual participants' systematic deviations from objective probabilities. The parieto-occipital cortex is thus a candidate neural substrate for humans' ability to approximate Bayesian inference by integrating prior beliefs with new information.

A Distinct Neural Code Supports Prospection of Future Probabilities During Instrumental Information-Seeking.

To make adaptive decisions, we must actively demand information, but relatively little is known about the mechanisms of active information gathering. An open question is how the brain estimates expected information gains (EIG) when comparing the current decision uncertainty with the uncertainty that is expected after gathering information. We examined this question using fMRI in a task in which people placed bids to obtain information in conditions that varied independently by prior decision uncertainty, information diagnosticity, and the penalty for an erroneous choice. Consistent with value of information theory, bids were sensitive to EIG and its components of prior certainty and expected posterior certainty. Expected posterior certainty was decoded above chance from multivoxel activation patterns in the posterior parietal and extrastriate cortices. This representation was independent of instrumental rewards and overlapped with distinct representations of EIG and prior certainty. Thus, posterior parietal and extrastriate cortices are candidates for mediating the prospection of posterior probabilities as a key step to estimate EIG during active information gathering.

Beta traveling waves in monkey frontal and parietal areas encode recent reward history.

Brain function depends on neural communication, but the mechanisms of this communication are not well understood. Recent studies suggest that one form of neural communication is through traveling waves (TWs)-patterns of neural oscillations that propagate within and between brain areas. We show that TWs are robust in microarray recordings in frontal and parietal cortex and encode recent reward history. Two adult male monkeys made saccades to obtain probabilistic rewards and were sensitive to the (statistically irrelevant) reward on the previous trial. TWs in frontal and parietal areas were stronger in trials that followed a prior reward versus a lack of reward and, in the frontal lobe, correlated with the monkeys' behavioral sensitivity to the prior reward. The findings suggest that neural communication mediated by TWs within the frontal and parietal lobes contribute to maintaining information about recent reward history and mediating the impact of this history on the monkeys' expectations.

Inefficient prioritization of task-relevant attributes during instrumental information demand.

In natural settings, people evaluate complex multi-attribute situations and decide which attribute to request information about. Little is known about how people make this selection and specifically, how they identify individual observations that best predict the value of a multi-attribute situation. Here show that, in a simple task of information demand, participants inefficiently query attributes that have high individual value but are relatively uninformative about a total payoff. This inefficiency is robust in two instrumental conditions in which gathering less informative observations leads to significantly lower rewards. Across individuals, variations in the sensitivity to informativeness is associated with personality metrics, showing negative associations with extraversion and thrill seeking and positive associations with stress tolerance and need for cognition. Thus, people select informative queries using sub-optimal strategies that are associated with personality traits and influence consequential choices.

A Reinforcement Meta-Learning framework of executive function and information demand.

Gathering information is crucial for maximizing fitness, but requires diverting resources from searching directly for primary rewards to actively exploring the environment. Optimal decision-making thus maximizes information while reducing effort costs, but little is known about the neuro-computational implementation of this tradeoff. We present a Reinforcement Meta-Learning (RML) computational model that solves the trade-off between the value and costs of gathering information. We implement the RML in a biologically plausible architecture that links catecholaminergic neuromodulators, the medial prefrontal cortex and topographically organized visual maps and show that it accounts for neural and behavioral findings on information demand motivated by instrumental incentives and intrinsic utility. Moreover, the utility function used by the RML, encoded by dopamine, is an approximation of variational free energy. Thus, the RML presents a biologically plausible mechanism for coordinating motivational, executive and sensory systems generate visual information gathering policies that minimize free energy.

Uncertainty modulates visual maps during noninstrumental information demand.

Animals are intrinsically motivated to obtain information independently of instrumental incentives. This motivation depends on two factors: a desire to resolve uncertainty by gathering accurate information and a desire to obtain positively-valenced observations, which predict favorable rather than unfavorable outcomes. To understand the neural mechanisms, we recorded parietal cortical activity implicated in prioritizing stimuli for spatial attention and gaze, in a task in which monkeys were free (but not trained) to obtain information about probabilistic non-contingent rewards. We show that valence and uncertainty independently modulated parietal neuronal activity, and uncertainty but not reward-related enhancement consistently correlated with behavioral sensitivity. The findings suggest uncertainty-driven and valence-driven information demand depend on partially distinct pathways, with the former being consistently related to parietal responses and the latter depending on additional mechanisms implemented in downstream structures.

Superstitious learning of abstract order from random reinforcement.

Humans and other animals often infer spurious associations among unrelated events. However, such superstitious learning is usually accounted for by conditioned associations, raising the question of whether an animal could develop more complex cognitive structures independent of reinforcement. Here, we tasked monkeys with discovering the serial order of two pictorial sets: a "learnable" set in which the stimuli were implicitly ordered and monkeys were rewarded for choosing the higher-rank stimulus and an "unlearnable" set in which stimuli were unordered and feedback was random regardless of the choice. We replicated prior results that monkeys reliably learned the implicit order of the learnable set. Surprisingly, the monkeys behaved as though some ordering also existed in the unlearnable set, showing consistent choice preference that transferred to novel untrained pairs in this set, even under a preference-discouraging reward schedule that gave rewards more frequently to the stimulus that was selected less often. In simulations, a model-free reinforcement learning algorithm (Q-learning) displayed a degree of consistent ordering among the unlearnable set but, unlike the monkeys, failed to do so under the preference-discouraging reward schedule. Our results suggest that monkeys infer abstract structures from objectively random events using heuristics that extend beyond stimulus-outcome conditional learning to more cognitive model-based learning mechanisms.

Humans monitor learning progress in curiosity-driven exploration.

Curiosity-driven learning is foundational to human cognition. By enabling humans to autonomously decide when and what to learn, curiosity has been argued to be crucial for self-organizing temporally extended learning curricula. However, the mechanisms driving people to set intrinsic goals, when they are free to explore multiple learning activities, are still poorly understood. Computational theories propose different heuristics, including competence measures (e.g., percent correct) and learning progress, that could be used as intrinsic utility functions to efficiently organize exploration. Such intrinsic utilities constitute computationally cheap but smart heuristics to prevent people from laboring in vain on unlearnable activities, while still motivating them to self-challenge on difficult learnable activities. Here, we provide empirical evidence for these ideas by means of a free-choice experimental paradigm and computational modeling. We show that while humans rely on competence information to avoid easy tasks, models that include a learning-progress component provide the best fit to task selection data. These results bridge the research in artificial and biological curiosity, reveal strategies that are used by humans but have not been considered in computational research, and introduce tools for probing how humans become intrinsically motivated to learn and acquire interests and skills on extended time scales.

Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network.

A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings. However, while computational theories predict that the benefits of new information depend on prior uncertainty, the cellular effects of uncertainty on the executive network are incompletely understood. Using simultaneous recordings in monkeys, we describe several mechanisms by which the fronto-parietal network reacts to uncertainty. We show that the variance of expected rewards, independently of the value of the rewards, was encoded in single neuron and population spiking activity and local field potential (LFP) oscillations, and, importantly, asymmetrically affected fronto-parietal information transmission (measured through the coherence between spikes and LFPs). Higher uncertainty selectively enhanced information transmission from the parietal to the frontal lobe and suppressed it in the opposite direction, consistent with Bayesian principles that prioritize sensory information according to a decision maker's prior uncertainty.

Parietal neurons encode information sampling based on decision uncertainty.

During natural behavior, animals actively gather information that is relevant for learning or actions; however, the mechanisms of active sampling are rarely investigated. We tested parietal neurons involved in oculomotor control in a task in which monkeys made saccades to gather visual information relevant to a subsequent action. We show that the neurons encode, before the saccade, the information gain (reduction in decision uncertainty) that the saccade was expected to bring for the following action. Sensitivity to information gain correlates with the monkeys' efficiency at processing the information in the post-saccadic fixation, but is independent of neuronal reward sensitivity. Reward sensitivity, in turn, is unreliable across task contexts, inconsistent with the view that the cells encode economic utility. The findings suggest that parietal cells involved in oculomotor decisions show uncertainty-dependent boosts of neural gain that facilitate the implementation of active sampling policies, including the selection of relevant cues and the efficient use of the information delivered by these cues.

Diverse motives for human curiosity.

Curiosity-our desire to know-is a fundamental drive in human behaviour, but its mechanisms are poorly understood. A classical question concerns the curiosity motives. What drives individuals to become curious about some but not other sources of information?1 Here we show that curiosity about probabilistic events depends on multiple aspects of the distribution of these events. Participants (n = 257) performed a task in which they could demand advance information about only one of two randomly selected monetary prizes that contributed to their income. Individuals differed markedly in the extent to which they requested information as a function of the ex ante uncertainty or ex ante value of an individual prize. This heterogeneity was not captured by theoretical models describing curiosity as a desire to learn about the total rewards of a situation2,3. Instead, it could be explained by an extended model that allowed for attribute-specific anticipatory utility-the savouring of individual components of the eventual reward-and postulates that this utility increased nonlinearly with the certainty of receiving the reward. Parameter values fitting individual choices were consistent for information about gains or losses, suggesting that attribute-specific anticipatory utility captures fundamental heterogeneity in the determinants of curiosity.

Towards a neuroscience of active sampling and curiosity.

In natural behaviour, animals actively interrogate their environments using endogenously generated 'question-and-answer' strategies. However, in laboratory settings participants typically engage with externally imposed stimuli and tasks, and the mechanisms of active sampling remain poorly understood. We review a nascent neuroscientific literature that examines active-sampling policies and their relation to attention and curiosity. We distinguish between information sampling, in which organisms reduce uncertainty relevant to a familiar task, and information search, in which they investigate in an open-ended fashion to discover new tasks. We review evidence that both sampling and search depend on individual preferences over cognitive states, including attitudes towards uncertainty, learning progress and types of information. We propose that, although these preferences are non-instrumental and can on occasion interfere with external goals, they are important heuristics that allow organisms to cope with the high complexity of both sampling and search, and generate curiosity-driven investigations in large, open environments in which rewards are sparse and ex ante unknown.

Understanding active sampling strategies: Empirical approaches and implications for attention and decision research.

In natural behavior we actively gather information using attention and active sensing behaviors (such as shifts of gaze) to sample relevant cues. However, while attention and decision making are naturally coordinated, in the laboratory they have been dissociated. Attention is studied independently of the actions it serves. Conversely, decision theories make the simplifying assumption that the relevant information is given, and do not attempt to describe how the decision maker may learn and implement active sampling policies. In this paper I review recent studies that address questions of attentional learning, cue validity and information seeking in humans and non-human primates. These studies suggest that learning a sampling policy involves large scale interactions between networks of attention and valuation, which implement these policies based on reward maximization, uncertainty reduction and the intrinsic utility of cognitive states. I discuss the importance of using such paradigms for formalizing the role of attention, as well as devising more realistic theories of decision making that capture a broader range of empirical observations.

Parietal neurons encode expected gains in instrumental information.

In natural behavior, animals have access to multiple sources of information, but only a few of these sources are relevant for learning and actions. Beyond choosing an appropriate action, making good decisions entails the ability to choose the relevant information, but fundamental questions remain about the brain's information sampling policies. Recent studies described the neural correlates of seeking information about a reward, but it remains unknown whether, and how, neurons encode choices of instrumental information, in contexts in which the information guides subsequent actions. Here we show that parietal cortical neurons involved in oculomotor decisions encode, before an information sampling saccade, the reduction in uncertainty that the saccade is expected to bring for a subsequent action. These responses were distinct from the neurons' visual and saccadic modulations and from signals of expected reward or reward prediction errors. Therefore, even in an instrumental context when information and reward gains are closely correlated, individual cells encode decision variables that are based on informational factors and can guide the active sampling of action-relevant cues.

Spatial and non-spatial aspects of visual attention: Interactive cognitive mechanisms and neural underpinnings.

In humans and non-human primates, the parietal lobe plays a key role in spatial attention - the ability to extract information from regions of space. This role is thought to be mediated by "priority" maps that highlight attention-worthy locations, and provide top-down feedback for motor orienting and attentional allocation. Traditionally, priority signals within the parietal cortex have been characterized as being purely spatial, i.e., encoding the desired locus of gaze or attention regardless of the context in which the brain generates that selection. Here, we highlight evidence from human behavior and neuroimaging as well as monkey physiology, to argue that non-spatial responses are critical to the establishment of priority maps in parietal cortex. This review offers an integrative view of the role that parietal cortex plays in attentional selection, providing evidence that priority maps reflect spatial and non-spatial priorities that ultimately act on sensory information in a spatial way.

Intrinsically motivated oculomotor exploration guided by uncertainty reduction and conditioned reinforcement in non-human primates.

Intelligent animals have a high degree of curiosity--the intrinsic desire to know--but the mechanisms of curiosity are poorly understood. A key open question pertains to the internal valuation systems that drive curiosity. What are the cognitive and emotional factors that motivate animals to seek information when this is not reinforced by instrumental rewards? Using a novel oculomotor paradigm, combined with reinforcement learning (RL) simulations, we show that monkeys are intrinsically motivated to search for and look at reward-predictive cues, and that their intrinsic motivation is shaped by a desire to reduce uncertainty, a desire to obtain conditioned reinforcement from positive cues, and individual variations in decision strategy and the cognitive costs of acquiring information. The results suggest that free-viewing oculomotor behavior reveals cognitive and emotional factors underlying the curiosity driven sampling of information.

Eye movements reveal epistemic curiosity in human observers.

Saccadic (rapid) eye movements are primary means by which humans and non-human primates sample visual information. However, while saccadic decisions are intensively investigated in instrumental contexts where saccades guide subsequent actions, it is largely unknown how they may be influenced by curiosity - the intrinsic desire to learn. While saccades are sensitive to visual novelty and visual surprise, no study has examined their relation to epistemic curiosity - interest in symbolic, semantic information. To investigate this question, we tracked the eye movements of human observers while they read trivia questions and, after a brief delay, were visually given the answer. We show that higher curiosity was associated with earlier anticipatory orienting of gaze toward the answer location without changes in other metrics of saccades or fixations, and that these influences were distinct from those produced by variations in confidence and surprise. Across subjects, the enhancement of anticipatory gaze was correlated with measures of trait curiosity from personality questionnaires. Finally, a machine learning algorithm could predict curiosity in a cross-subject manner, relying primarily on statistical features of the gaze position before the answer onset and independently of covariations in confidence or surprise, suggesting potential practical applications for educational technologies, recommender systems and research in cognitive sciences. With this article, we provide full access to the annotated database allowing readers to reproduce the results. Epistemic curiosity produces specific effects on oculomotor anticipation that can be used to read out curiosity states.

A Multi-Area Stochastic Model for a Covert Visual Search Task.

Decisions typically comprise several elements. For example, attention must be directed towards specific objects, their identities recognized, and a choice made among alternatives. Pairs of competing accumulators and drift-diffusion processes provide good models of evidence integration in two-alternative perceptual choices, but more complex tasks requiring the coordination of attention and decision making involve multistage processing and multiple brain areas. Here we consider a task in which a target is located among distractors and its identity reported by lever release. The data comprise reaction times, accuracies, and single unit recordings from two monkeys' lateral interparietal area (LIP) neurons. LIP firing rates distinguish between targets and distractors, exhibit stimulus set size effects, and show response-hemifield congruence effects. These data motivate our model, which uses coupled sets of leaky competing accumulators to represent processes hypothesized to occur in feature-selective areas and limb motor and pre-motor areas, together with the visual selection process occurring in LIP. Model simulations capture the electrophysiological and behavioral data, and fitted parameters suggest that different connection weights between LIP and the other cortical areas may account for the observed behavioral differences between the animals.

Attention, reward, and information seeking.

Decision making is thought to be guided by the values of alternative options and involve the accumulation of evidence to an internal bound. However, in natural behavior, evidence accumulation is an active process whereby subjects decide when and which sensory stimulus to sample. These sampling decisions are naturally served by attention and rapid eye movements (saccades), but little is known about how saccades are controlled to guide future actions. Here we review evidence that was discussed at a recent symposium, which suggests that information selection involves basal ganglia and cortical mechanisms and that, across different contexts, it is guided by two central factors: the gains in reward and gains in information (uncertainty reduction) associated with sensory cues.