# Publications

Forthcoming
Weber, I., Zorowitz, S., Niv, Y., & Bennett, D. ﻿. (Forthcoming). The effects of induced positive and negative affect on Pavlovian-instrumental interactions. Cognition and Emotion. PreprintAbstract
Across species, animals have an intrinsic drive to approach appetitive stimuli and to withdraw from aversive stimuli. In affective science, influential theories of emotion link positive affect with strengthened behavioral approach and negative affect with avoidance. Based on these theories, we predicted that individuals’ positive and negative affect levels should particularly influence their behavior when innate Pavlovian approach/avoidance tendencies conflict with learned instrumental behaviors. Here, across two experiments—exploratory Experiment 1 (N = 91) and a preregistered confirmatory Experiment 2 (N = 335)—we assessed how induced positive and negative affect influenced Pavlovian-instrumental interactions in a reward/punishment Go/No-Go task. Contrary to our hypotheses, we found no evidence for a main effect of positive/negative affect on either approach/avoidance behavior or Pavlovian-instrumental interactions. However, we did find evidence that the effects of induced affect on behavior were moderated by individual differences in self-reported behavioral inhibition and gender. Exploratory computational modelling analyses explained these demographic moderating effects as arising from positive correlations between demographic factors and individual differences in the strength of Pavlovian-instrumental interactions. These findings serve to sharpen our understanding of the effects of positive and negative affect on instrumental behavior.
Bennett, D., Radulescu, A., Zorowitz, S., Felso, V., & Niv, Y. (Forthcoming). Affect-congruent attention drives changes in reward expectations. PreprintAbstract
Positive and negative affective states are respectively associated with optimistic and pessimistic expectations regarding future reward. One mechanism that might underlie these affect-related expectation biases is attention to positive- versus negative-valence stimulus features (e.g., attending to the positive reviews of a restaurant versus its expensive price). Here we tested the effects of experimentally induced positive and negative affect on feature-based attention in 120 participants completing a compound-generalization task with eye-tracking. We found that participants' reward expectations for novel compound stimuli were modulated by the affect induction in an affect-congruent way: positive affect increased reward expectations for compounds, whereas negative affect decreased reward expectations. Computational modelling and eye-tracking analyses each revealed that these effects were driven by affect-congruent changes in participants' allocation of attention to high- versus low-value features of compound stimuli. These results provide mechanistic insight into a process by which affect produces biases in generalized reward expectations.
Zorowitz, S., Niv, Y., & Bennett, D. (Forthcoming). Inattentive responding can induce spurious associations between task behavior and symptom measures. PreprintAbstract

2022
Song, M., Jones, C. E., Monfils, M. - H., & Niv, Y. (2022). Explaining the effectiveness of fear extinction through latent-cause inference. Neurons, Behavior, Data analysis, and Theory. PDFAbstract
Acquiring fear responses to predictors of aversive outcomes is crucial for survival. At the same time, it is important to be able to modify such associations when they are maladaptive, for instance in treating anxiety and trauma-related disorders. Standard extinction procedures can reduce fear temporarily, but with sufficient delay or with reminders of the aversive experience, fear often returns. The latent-cause inference framework explains the return of fear by presuming that animals learn a rich model of the environment, in which the standard extinction procedure triggers the inference of a new latent cause, preventing the unlearning of the original aversive associations. This computational framework had previously inspired an alternative extinction paradigm – gradual extinction – which indeed was shown to be more effective in reducing the return of fear. However, the original framework was not sufficient to explain the pattern of results seen in the experiments. Here, we propose a formal model to explain the effectiveness of gradual extinction in reducing spontaneous recovery and reinstatement effects, in contrast to the ineffectiveness of standard extinction and a gradual reverse control procedure. We demonstrate through quantitative simulation that our model can explain qualitative behavioral differences across different extinction procedures as seen in the empirical study. We verify the necessity of several key assumptions added to the latent-cause framework, which suggest potential general principles of animal learning and provide novel predictions for future experiments.
Song, M., Takahashi, Y. K., Burton, A. C., Roesch, M. R., Schoenbaum, G., Niv, Y., & Langdon, A. J. (2022). Minimal cross-trial generalization in learning the representation of an odor-guided choice task. PLOS Computational Biology , 18 (3). PDFAbstract
Langdon, A., Botvinick, M., Nakahara, H., Tanaka, K., Matsumoto, M., & Kanai, R. (2022). Meta-learning, social cognition and consciousness in brains and machines. Neural Networks , 145, 80-89. PDFAbstract
The intersection between neuroscience and artificial intelligence (AI) research has created synergistic effects in both fields. While neuroscientific discoveries have inspired the development of AI architectures, new ideas and algorithms from AI research have produced new ways to study brain mechanisms. A well-known example is the case of reinforcement learning (RL), which has stimulated neuroscience research on how animals learn to adjust their behavior to maximize reward. In this review article, we cover recent collaborative work between the two fields in the context of meta-learning and its extension to social cognition and consciousness. Meta-learning refers to the ability to learn how to learn, such as learning to adjust hyperparameters of existing learning algorithms and how to use existing models and knowledge to efficiently solve new tasks. This meta-learning capability is important for making existing AI systems more adaptive and flexible to efficiently solve new tasks. Since this is one of the areas where there is a gap between human performance and current AI systems, successful collaboration should produce new ideas and progress. Starting from the role of RL algorithms in driving neuroscience, we discuss recent developments in deep RL applied to modeling prefrontal cortex functions. Even from a broader perspective, we discuss the similarities and differences between social cognition and meta-learning, and finally conclude with speculations on the potential links between intelligence as endowed by model-based RL and consciousness. For future work we highlight data efficiency, autonomy and intrinsic motivation as key research areas for advancing both fields.
2021
Niv, Y., Hitchcock, P., Berwian, I. M., & Schoen, G. (2021). Toward Precision Cognitive Behavioral Therapy via Reinforcement Learning Theory (Ch. 12). In LM Williams and LM Hacks (Eds). Precision Psychiatry . American Psychiatric Association. Publisher's Version
Eldar*, E., Felso*, V., Cohen, J. D., & Niv, Y. (2021). A pupillary index of susceptibility to decision biases. Nature Human Behavior. Publisher's VersionAbstract
The demonstration that human decision-making can systematically violate the laws of rationality has had a wide impact on behavioural sciences. In this study, we use a pupillary index to adjudicate between two existing hypotheses about how irrational biases emerge: the hypothesis that biases result from fast, effortless processing and the hypothesis that biases result from more extensive integration. While effortless processing is associated with smaller pupillary responses, more extensive integration is associated with larger pupillary responses. Thus, we tested the relationship between pupil response and choice behaviour on six different foundational decision-making tasks that are classically used to demonstrate irrational biases. Participants demonstrated the expected systematic biases and their pupillary measurements satisfied pre-specified quality checks. Planned analyses returned inconclusive results, but exploratory examination of the data revealed an association between high pupillary responses and biased decisions. The findings provide preliminary support for the hypothesis that biases arise from gradual information integration.
Bennett, D., Niv, Y., & Langdon, A. J. (2021). Value-free reinforcement learning: policy optimization as a minimal model of operant behavior. Current Opinion in Behavioral Sciences , 41, 114–121. PDFAbstract

Reinforcement learning is a powerful framework for modelling the cognitive and neural substrates of learning and decision making. Contemporary research in cognitive neuroscience and neuroeconomics typically uses value-based reinforcement-learning models, which assume that decision-makers choose by comparing learned values for different actions. However, another possibility is suggested by a simpler family of models, called policy-gradient reinforcement learning. Policy-gradient models learn by optimizing a behavioral policy directly, without the intermediate step of value-learning. Here we review recent behavioral and neural findings that are more parsimoniously explained by policy-gradient models than by value-based models. We conclude that, despite the ubiquity of ‘value’ in reinforcement-learning models of decision making, policy-gradient models provide a lightweight and compelling alternative model of operant behavior.

Shin, Y. S., & Niv, Y. (2021). Biased evaluations emerge from inferring hidden causes. Nature Human Behaviour. PDFAbstract
How do we evaluate a group of people after a few negative experiences with some members but mostly positive experiences otherwise? How do rare experiences influence our overall impression? We show that rare events may be overweighted due to normative inference of the hidden causes that are believed to generate the observed events. We propose a Bayesian inference model that organizes environmental statistics by combining similar events and separating outlying observations. Relying on the model’s inferred latent causes for group evaluation overweights rare or variable events. We tested the model’s predictions in eight experiments where participants observed a sequence of social or non-social behaviours and estimated their average. As predicted, estimates were biased toward sparse events when estimating after seeing all observations, but not when tracking a summary value as observations accrued. Our results suggest that biases in evaluation may arise from inferring the hidden causes of group members’ behaviours.
Hitchcock, P., Forman, E., Rothstein, N., Zhang, F., Kounios, J., Niv, Y., & Sims, C. (2021). Rumination derails reinforcement learning with possible implications for ineffective behavior. Clinical Psychological Science. PDFAbstract

How does rumination affect reinforcement learning — the ubiquitous process by which we adjust behavior after error in order to behave more effectively in the future? In a within-subject design (n=49), we tested whether experimentally induced rumination disrupts reinforcement learning in a multidimensional learning task previously shown to rely on selective attention. Rumination impaired performance, yet unexpectedly this impairment could not be attributed to decreased attentional breadth (quantified using a “decay” parameter in a computational model). Instead, trait rumination (between subjects) was associated with higher decay rates (implying narrower attention), yet not with impaired performance. Our task-performance results accord with the possibility that state rumination promotes stress-generating behavior in part by disrupting reinforcement learning. The trait-rumination finding accords with the predictions of a prominent model of trait rumination (the attentional-scope model). More work is needed to understand the specific mechanisms by which state rumination disrupts reinforcement learning.

Zorowitz, S., Bennett, D., Choe, G., & Niv, Y. (2021). A Recurring Reproduction Error in the Administration of the Generalized Anxiety Disorder Scale. Lancet Psychiatry. PDF
Rouhani, N., & Niv, Y. (2021). Signed and unsigned reward prediction errors dynamically enhance learning and memory. eLife , 10 (e61077). Publisher's VersionAbstract
Memory helps guide behavior, but which experiences from the past are prioritized? Classic models of learning posit that events associated with unpredictable outcomes as well as, paradoxically, predictable outcomes, deploy more attention and learning for those events. Here, we test reinforcement learning and subsequent memory for those events, and treat signed and unsigned reward prediction errors (RPEs), experienced at the reward-predictive cue or reward outcome, as drivers of these two seemingly contradictory signals. By fitting reinforcement learning models to behavior, we find that both RPEs contribute to learning by modulating a dynamically changing learning rate. We further characterize the effects of these RPE signals on memory, and show that both signed and unsigned RPEs enhance memory, in line with midbrain dopamine and locus-coeruleus modulation of hippocampal plasticity, thereby reconciling separate findings in the literature.
Radulescu, A., Shin, Y. S., & Niv, Y. (2021). Human representation learning. Annual Reviews in Neuroscience. PDFAbstract

The central theme of this review is the dynamic interaction between infor- mation selection and learning. We pose a fundamental question about this interaction: How do we learn what features of our experiences are worth learning about? In humans, this process depends on attention and memory, two cognitive functions that together constrain representations of the world to features that are relevant for goal attainment. Recent evidence suggests that the representations shaped by attention and memory are themselves in- ferred from experience with each task. We review this evidence and place it in the context of work that has explicitly characterized representation learning as statistical inference. We discuss how inference can be scaled to real-world decisions by approximating beliefs based on a small number of experiences. Finally, we highlight some implications of this inference process for human decision-making in social environments.

Niv, Y. (2021). The primacy of behavioral research for understanding the brain. Behavioral Neuroscience. PDFAbstract

Understanding the brain requires us to answer both what the brain does, and how it does it. Using a series of examples, I make the case that behavior is often more useful than neuroscientific measurements for answering the first question. Moreover, I show that even for “how” questions that pertain to neural mechanism, a well-crafted behavioral paradigm can offer deeper insight and stronger constraints on computational and mechanistic models than do many highly challenging (and very expensive) neural studies. I conclude that behavioral, rather than neuroscientific research, is essential for understanding the brain, contrary to the opinion of prominent funding bodies and scientific journals, who erroneously place neural data on a pedestal and consider behavior to be subsidiary.

Hayden, B. Y., & Niv, Y. (2021). The case against economic values in the orbitofrontal cortex (or anywhere else in the brain). Behavioral Neuroscience , 135 (2), 192-201. PreprintAbstract

Much of traditional neuroeconomics proceeds from the hypothesis that value is reified in the brain, that is, that there are neurons or brain regions whose responses serve the discrete purpose of encoding value. This hypothesis is supported by the finding that the activity of many neurons covaries with subjective value as estimated in specific tasks and has led to the idea that the primary function of the orbitofrontal cortex is to compute and signal economic value. Here we consider an alternative: that economic value, in the cardinal, common-currency sense, is not represented in the brain and used for choice by default. This idea is motivated by consideration of the economic concept of value, which places important epistemic constraints on our ability to identify its neural basis. It is also motivated by the behavioral economics literature, especially work on heuristics, which proposes value-free process models for much if not all of choice. Finally, it is buoyed by recent neural and behavioral findings regarding how animals and humans learn to choose between options. In light of our hypothesis, we critically reevaluate putative neural evidence for the representation of value and explore an alternative: direct learning of action policies. We delineate how this alternative can provide a robust account of behavior that concords with existing empirical data.

The accepted manuscript version of this article will be publicly available on 05/31/2022.
Chan, S. C. Y., Schuck, N. W., Lopatina, N., Schoenbaum, G., & Niv, Y. (2021). Orbitofrontal cortex and learning predictions of state transitions. Behavioral Neuroscience. PDFAbstract
Learning the transition structure of the environment – the probabilities of transitioning from one environmental state to another – is a key prerequisite for goal-directed planning and model-based decision making. To investigate the role of the orbitofrontal cortex (OFC) in goal-directed planning and decision making, we used fMRI to assess univariate and multivariate activity in the OFC while humans experienced state transitions that varied in degree of surprise. In convergence with recent evidence, we found that OFC activity was related to greater learning about transition structure, both across subjects and on a trial-by-trial basis. However, this relationship was inconsistent with a straightforward interpretation of OFC activity as representing a state prediction error that would facilitate learning of transitions via error-correcting mechanisms. The state prediction error hypothesis predicts that OFC activity at the time of observing an outcome should increase expectation of that observed outcome on subsequent trials. Instead, our results showed that OFC activity was associated with increased expectation of the more probable outcome; that is, with more optimal predictions. Our findings add to the evidence of OFC involvement in learning state-to-state transition structure, while providing new constraints for algorithmic hypotheses regarding how these transitions are learned.
Langdon, A. J., & Chaudhuri, R. (2021). An evolving perspective on the dynamic brain: notes from the Brain Conference on Dynamics of the brain: temporal aspects of computation. European Journal of Neuroscience. PDF
Bennett, D., Davidson, G., & Niv, Y. (2021). A model of mood as integrated advantage. Psychological Review. PreprintAbstract
Mood is an integrative and diffuse affective state that is thought to exert a pervasive effect on cognition and behavior. At the same time, mood itself is thought to fluctuate slowly as a product of feedback from interactions with the environment. Here we present a new computational theory of the valence of mood—the Integrated Advantage model—that seeks to account for this bidirectional interaction. Adopting theoretical formalisms from reinforcement learning, we propose to conceptualize the valence of mood as a leaky integral of an agent’s appraisals of the Advantage of its actions. This model generalizes and extends previous models of mood wherein affective valence was conceptualized as a moving average of reward prediction errors. We give a full theoretical derivation of the Integrated Advantage model and provide a functional explanation of how an integrated-Advantage variable could be deployed adaptively by a biological agent to accelerate learning in complex and/or stochastic environments. Specifically, drawing on stochastic optimization theory, we propose that an agent can utilize our hypothesized form of mood to approximate a momentum-based update to its behavioral policy, thereby facilitating rapid learning of optimal actions. We then show how this model of mood provides a principled and parsimonious explanation for a number of contextual effects on mood from the affective science literature, including expectation- and surprise-related effects, counterfactual effects from information about foregone alternatives, action-typicality effects, and action/inaction asymmetry.
The accepted manuscript version of this article will be publicly available on 09/13/2022.
2020
Daniel, R., Radulescu, A., & Niv, Y. (2020). Intact reinforcement learning but impaired attentional control during multidimensional probabilistic learning in older adults. Journal of Neuroscience , 40(5), 1084-1096. PDFAbstract

attentional task demands, and the level of suppression correlated with behavioral performance. Our results indicate that healthy aging does not signicantly impair simple reinforcement learning. However, in complex environments, older adults rely more heavily on suboptimal reinforcement-learning strategies supported by the ventral striatum, whereas younger adults utilize attention processes supported by cortical networks.

Drummond, N., & Niv, Y. (2020). Model-based decision making and model-free learning. Current Biology , 30 (15), 860-865. PDFAbstract
Free will is anything but free. With it comes the onus of choice: not only what to do, but which inner voice to listen to — our ‘automatic’ response system, which some consider ‘impulsive’ or ‘irrational’, or our supposedly more rational deliberative one. Rather than a devil and angel sitting on our shoulders, research suggests that we have two decision-making systems residing in the brain, in our basal ganglia. Neither system is the devil and neither is irrational. They both have our best interests at heart and aim to suggest the best course of action calculated through rational algorithms. However, the algorithms they use are qualitatively different and do not always agree on which action is optimal. The rivalry between habitual, fast action and deliberative, purposeful action is an ongoing one.
Rouhani, N., Norman, K. A., Niv, Y., & Bornstein, A. M. (2020). Reward prediction errors create event boundaries in memory. Cognition. PDFAbstract
We remember when things change. Particularly salient are experiences where there is a change in rewards, eliciting reward prediction errors (RPEs). How do RPEs influence our memory of those experiences? One idea is that this signal directly enhances the encoding of memory. Another, not mutually exclusive, idea is that the RPE signals a deeper change in the environment, leading to the mnemonic separation of subsequent experiences from what came before, thereby creating a new latent context and a more separate memory trace. We tested this in four experiments where participants learned to predict rewards associated with a series of trial-unique images. High-magnitude RPEs indicated a change in the underlying distribution of rewards. To test whether these large RPEs created a new latent context, we first assessed recognition priming for sequential pairs that included a high-RPE event or not (Exp. 1: n = 27 & Exp. 2: n = 83). We found evidence of recognition priming for the high-RPE event, indicating that the high-RPE event is bound to its predecessor in memory. Given that high-RPE events are themselves preferentially remembered (Rouhani, Norman, & Niv, 2018), we next tested whether there was an event boundary across a high-RPE event (i.e., excluding the high-RPE event itself; Exp. 3: n = 85). Here, sequential pairs across a high RPE no longer showed recognition priming whereas pairs within the same latent reward state did, providing initial evidence for an RPE-modulated event boundary. We then investigated whether RPE event boundaries disrupt temporal memory by asking participants to order and estimate the distance between two events that had either included a high-RPE event between them or not (Exp. 4). We found (n = 49) and replicated (n = 77) worse sequence memory for events across a high RPE. In line with our recognition priming results, we did not find sequence memory to be impaired between the high-RPE event and its predecessor, but instead found worse sequence memory for pairs across a high-RPE event. Moreover, greater distance between events at encoding led to better sequence memory for events across a low-RPE event, but not a high-RPE event, suggesting separate mechanisms for the temporal ordering of events within versus across a latent reward context. Altogether, these findings demonstrate that high-RPE events are both more strongly encoded, show intact links with their predecessor, and act as event boundaries that interrupt the sequential integration of events. We captured these effects in a variant of the Context Maintenance and Retrieval model (CMR; Polyn, Norman, & Kahana, 2009), modified to incorporate RPEs into the encoding process.
Cai, M. B., Shvartsman, M., Wu, A., Zhang, H., & Ju, X. (2020). Incorporating structured assumptions with probabilistic graphical models in fMRI data analysis. Neuropsychologia. Publisher's VersionAbstract
With the wide adoption of functional magnetic resonance imaging (fMRI) by cognitive neuroscience researchers, large volumes of brain imaging data have been accumulated in recent years. Aggregating these data to derive scientific insights often faces the challenge that fMRI data are high-dimensional, heterogeneous across people, and noisy. These challenges demand the development of computational tools that are tailored both for the neuroscience questions and for the properties of the data. We review a few recently developed algorithms in various domains of fMRI research: fMRI in naturalistic tasks, analyzing full-brain functional connectivity, pattern classification, inferring representational similarity and modeling structured residuals. These algorithms all tackle the challenges in fMRI similarly: they start by making clear statements of assumptions about neural data and existing domain knowledge, incorporate those assumptions and domain knowledge into probabilistic graphical models, and use those models to estimate properties of interest or latent structures in the data. Such approaches can avoid erroneous findings, reduce the impact of noise, better utilize known properties of the data, and better aggregate data across groups of subjects. With these successful cases, we advocate wider adoption of explicit model construction in cognitive neuroscience. Although we focus on fMRI, the principle illustrated here is generally applicable to brain data of other modalities.
Langdon, A. J., & Daw, N. (2020). Beyond the Average View of Dopamine. Trends in Cognitive Sciences. PDFAbstract
Dopamine (DA) responses are synonymous with the ‘reward prediction error’ of reinforcement learning (RL), and are thought to update neural estimates of expected value. A recent study by Dabney et al. enriches this picture, demonstrating that DA neurons track variability in rewards, providing a readout of risk in the brain.
Sharpe, M. J., Batchelor, H. M., Mueller, L. E., Chang, C. Y., Maes, E. J. P., Niv, Y., & Schoenbaum, G. (2020). Dopamine transients do not act as model-free prediction errors during associative learning. Nature Communications , 11 (1), 106. Publisher's VersionAbstract
Dopamine neurons are proposed to signal the reward prediction error in model-free reinforcement learning algorithms. This term represents the unpredicted or ‘excess’ value of the rewarding event, value that is then added to the intrinsic value of any antecedent cues, contexts or events. To support this proposal, proponents cite evidence that artificially-induced dopamine transients cause lasting changes in behavior. Yet these studies do not generally assess learning under conditions where an endogenous prediction error would occur. Here, to address this, we conducted three experiments where we optogenetically activated dopamine neurons while rats were learning associative relationships, both with and without reward. In each experiment, the antecedent cues failed to acquire value and instead entered into associations with the later events, whether valueless cues or valued rewards. These results show that in learning situations appropriate for the appearance of a prediction error, dopamine transients support associative, rather than model-free, learning.
2019
Bravo-Hermsdorff, G., Felso, V., Ray, E., Gunderson, L. M., Helander, M. E., Maria, J., & Niv, Y. (2019). Gender and collaboration patterns in a temporal scientific authorship network. Applied Network Science , 4 (1), 112. Publisher's VersionAbstract
One can point to a variety of historical milestones for gender equality in STEM (science, technology, engineering, and mathematics), however, practical effects are incremental and ongoing. It is important to quantify gender differences in subdomains of scientific work in order to detect potential biases and monitor progress. In this work, we study the relevance of gender in scientific collaboration patterns in the Institute for Operations Research and the Management Sciences (INFORMS), a professional society with sixteen peer-reviewed journals. Using their publication data from 1952 to 2016, we constructed a large temporal bipartite network between authors and publications, and augmented the author nodes with gender labels. We characterized differences in several basic statistics of this network over time, highlighting how they have changed with respect to relevant historical events. We find a steady increase in participation by women (e.g., fraction of authorships by women and of new women authors) starting around 1980. However, women still comprise less than 25% of the INFORMS society and an even smaller fraction of authors with many publications. Moreover, we describe a methodology for quantifying the structural role of an authorship with respect to the overall connectivity of the network, using it to measure subtle differences between authorships by women and by men. Specifically, as measures of structural importance of an authorship, we use effective resistance and contraction importance, two measures related to diffusion throughout a network. As a null model, we propose a degree-preserving temporal and geometric network model with emergent communities. Our results suggest the presence of systematic differences between the collaboration patterns of men and women that cannot be explained by only local statistics.
Niv, Y. (2019). Learning task-state representations. Nature Neuroscience , 22 (10), 1544–1553. PDFAbstract
Arguably, the most difficult part of learning is deciding what to learn about. Should I associate the positive outcome of safely completing a street-crossing with the situation ‘the car approaching the crosswalk was red' or with ‘the approaching car was slowing down'? In this Perspective, we summarize our recent research into the computational and neural underpinnings of ‘representation learning'—how humans (and other animals) construct task representations that allow efficient learning and decision-making. We first discuss the problem of learning what to ignore when confronted with too much information, so that experience can properly generalize across situations. We then turn to the problem of augmenting perceptual information with inferred latent causes that embody unobservable task-relevant information, such as contextual knowledge. Finally, we discuss recent findings regarding the neural substrates of task representations that suggest the orbitofrontal cortex represents ‘task states', deploying them for decision-making and learning elsewhere in the brain.
Schuck, N. W., & Niv, Y. (2019). Sequential replay of nonspatial task states in the human hippocampus. Science. Publisher's VersionAbstract
Sequential neural activity patterns related to spatial experiences are “replayed” in the hippocampus of rodents during rest. We investigated whether replay of nonspatial sequences can be detected noninvasively in the human hippocampus. Participants underwent functional magnetic resonance imaging (fMRI) while resting after performing a decision-making task with sequential structure. Hippocampal fMRI patterns recorded at rest reflected sequentiality of previously experienced task states, with consecutive patterns corresponding to nearby states. Hippocampal sequentiality correlated with the fidelity of task representations recorded in the orbitofrontal cortex during decision-making, which were themselves related to better task performance. Our findings suggest that hippocampal replay may be important for building representations of complex, abstract tasks elsewhere in the brain and establish feasibility of investigating fast replay signals with fMRI.
Rouhani, N., & Niv, Y. (2019). Depressive symptoms bias the prediction-error enhancement of memory towards negative events in reinforcement learning. Psychopharmacology , 236 (8), 2425–2435. PDFAbstract

Rationale. Depression is a disorder characterized by sustained negative affect and blunted positive affect, suggesting potential abnormalities in reward learning and its interaction with episodic memory. Objectives. This study investigated how reward prediction errors experienced during learning modulate memory for rewarding events in individuals with depressive and non-depressive symptoms.

Methods. Across three experiments, participants learned the average values of two scene categories in two learning contexts. Each learning context had either high or low outcome variance, allowing us to test the effects of small and large prediction errors on learning and memory. Participants were later tested for their memory of trial-unique scenes that appeared alongside outcomes. We compared learning and memory performance of individuals with self-reported depressive symptoms (N = 101) to those without (N = 184).

Results. Although there were no overall differences in reward learning between the depressive and non-depressive group, depression severity within the depressive group predicted greater error in estimating the values of the scene categories. Similarly, there were no overall differences in memory performance. However, in depressive participants, negative prediction errors enhanced episodic memory more so than did positive prediction errors, and vice versa for non-depressive participants who showed a larger effect of positive prediction errors on memory. These results reflected differences in memory both within group and across groups.

Conclusions. Individuals with self-reported depressive symptoms showed relatively intact reinforcement learning, but demonstrated a bias for encoding events that accompanied surprising negative outcomes versus surprising positive ones. We discuss a potential neural mechanism supporting these effects, which may underlie or contribute to the excessive negative affect observed in depression.

Sharpe, M. J., Batchelor, H. M., Mueller, L. E., Chang, C. Y., Maes, E. J. P., Niv, Y., & Schoenbaum, G. (2019). Dopamine transients delivered in learning contexts do not act as model-free prediction errors. bioRxiv. PDFAbstract
Dopamine neurons fire transiently in response to unexpected rewards. These neural correlates are proposed to signal the reward prediction error described in model-free reinforcement learning algorithms. This error term represents the unpredicted or excess value of the rewarding event. In model-free reinforcement learning, this value is then stored as part of the learned value of any antecedent cues, contexts or events, making them intrinsically valuable, independent of the specific rewarding event that caused the prediction error. In support of equivalence between dopamine transients and this model-free error term, proponents cite causal optogenetic studies showing that artificially induced dopamine transients cause lasting changes in behavior. Yet none of these studies directly demonstrate the presence of cached value under conditions appropriate for associative learning. To address this gap in our knowledge, we conducted three studies where we optogenetically activated dopamine neurons while rats were learning associative relationships, both with and without reward. In each experiment, the antecedent cues failed to acquired value and instead entered into value-independent associative relationships with the other cues or rewards. These results show that dopamine transients, constrained within appropriate learning situations, support valueless associative learning.
Radulescu, A., Niv, Y., & Ballard, I. (2019). Holistic Reinforcement Learning: The Role of Structure and Attention. Trends in Cognitive Sciences. PDFAbstract
Compact representations of the environment allow humans to behave efficiently in a complex world. Reinforcement learning models capture many behavioral and neural effects but do not explain recent findings showing that structure in the environment influences learning. In parallel, Bayesian cognitive models predict how humans learn structured knowledge but do not have a clear neurobiological implementation. We propose an integration of these two model classes in which structured knowledge learned via approximate Bayesian inference acts as a source of selective attention. In turn, selective attention biases reinforcement learning towards relevant dimensions of the environment. An understanding of structure learning will help to resolve the fundamental challenge in decision science: explaining why people make the decisions they do.
McDougle, S. D., Butcher, P. A., Parvin, D. E., Mushtaq, F., Niv, Y., Ivry, R. B., & Taylor, J. A. (2019). Neural Signatures of Prediction Errors in a Decision-Making Task Are Modulated by Action Execution Failures. Current Biology. PDFAbstract
Decisions must be implemented through actions, and actions are prone to error. As such, when an expected outcome is not obtained, an individual should be sensitive to not only whether the choice itself was suboptimal but also whether the action required to indicate that choice was executed successfully. The intelligent assignment of credit to action execution versus action selection has clear ecological utility for the learner. To explore this, we used a modified version of a classic reinforcement learning task in which feedback indicated whether negative prediction errors were, or were not, associated with execution errors. Using fMRI, we asked if prediction error computations in the human striatum, a key substrate in reinforcement learning and decision making, are modulated when a failure in action execution results in the negative outcome. Participants were more tolerant of non-rewarded outcomes when these resulted from execution errors versus when execution was successful, but reward was withheld. Consistent with this behavior, a model-driven analysis of neural activity revealed an attenuation of the signal associated with negative reward prediction errors in the striatum following execution failures. These results converge with other lines of evidence suggesting that prediction errors in the mesostriatal dopamine system integrate high-level information during the evaluation of instantaneous reward outcomes.
Zhou, J., Gardner, M. P. H., Stalnaker, T. A., Ramus, S. J., Wikenheiser, A. M., Niv, Y., & Schoenbaum, G. (2019). Rat Orbitofrontal Ensemble Activity Contains Multiplexed but Dissociable Representations of Value and Task Structure in an Odor Sequence Task. Current Biology , 29 (6), 897–907.e3. PDFAbstract
The orbitofrontal cortex (OFC) has long been implicated in signaling information about expected outcomes to facilitate adaptive or flexible behavior. Current proposals focus on signaling of expected value versus the representation of a value-agnostic cognitive map of the task. While often suggested as mutually exclusive, these alternatives may represent extreme ends of a continuum determined by task complexity and experience. As learning proceeds, an initial, detailed cognitive map might be acquired, based largely on external information. With more experience, this hypothesized map can then be tailored to include relevant abstract hidden cognitive constructs. The map would default to an expected value in situations where other attributes are largely irrelevant, but, in richer tasks, a more detailed structure might continue to be represented, at least where relevant to behavior. Here, we examined this by recording single-unit activity from the OFC in rats navigating an odor sequence task analogous to a spatial maze. The odor sequences provided a mappable state space, with 24 unique “positions” defined by sensory information, likelihood of reward, or both. Consistent with the hypothesis that the OFC represents a cognitive map tailored to the subjects' intentions or plans, we found a close correspondence between how subjects were using the sequences and the neural representations of the sequences in OFC ensembles. Multiplexed with this value-invariant representation of the task, we also found a representation of the expected value at each location. Thus, the value and task structure co-existed as dissociable components of the neural code in OFC.
Langdon, A. J., Hathaway, B. A., Zorowitz, S., Harris, C. B. W., & Winstanley, C. A. (2019). Relative insensitivity to time-out punishments induced by win-paired cues in a rat gambling task. Psychopharmacology , 236 (8), 2543–2556. PDFAbstract
Rationale. Pairing rewarding outcomes with audiovisual cues in simulated gambling games increases risky choice in both humans and rats. However, the cognitive mechanism through which this sensory enhancement biases decision-making is unknown. Objectives. To assess the computational mechanisms that promote risky choice during gambling, we applied a series of reinforcement learning models to a large dataset of choices acquired from rats as they each performed one of two variants of a rat gambling task (rGT), in which rewards on “win” trials were delivered either with or without salient audiovisual cues. Methods. We used a sampling technique based on Markov chain Monte Carlo to obtain posterior estimates of model parameters for a series of RL models of increasing complexity, in order to assess the relative contribution of learning about positive and negative outcomes to the latent valuation of each choice option on the cued and uncued rGT. Results. Rats which develop a preference for the risky options on the rGT substantially down-weight the equivalent cost of the time-out punishments during these tasks. For each model tested, the reduction in learning from the negative time-outs correlated with the degree of risk preference in individual rats. We found no apparent relationship between risk preference and the parameters that govern learning from the positive rewards. Conclusions. The emergence of risk-preferring choice on the rGT derives from a relative insensitivity to the cost of the time-out punishments, as opposed to a relative hypersensitivity to rewards. This hyposensitivity to punishment is more likely to be induced in individual rats by the addition of salient audiovisual cues to rewards delivered on win trials.
Cai, M. B., Schuck, N. W., Pillow, J. W., & Niv, Y. (2019). Representational structure or task structure? Bias in neural representational similarity analysis and a Bayesian method for reducing bias. PLoS computational biology. PDFAbstract
The activity of neural populations in the brains of humans and animals can exhibit vastly different spatial patterns when faced with different tasks or environmental stimuli. The degrees of similarity between these neural activity patterns in response to different events are used to characterize the representational structure of cognitive states in a neural population. The dominant methods of investigating this similarity structure first estimate neural activity patterns from noisy neural imaging data using linear regression, and then examine the similarity between the estimated patterns. Here, we show that this approach introduces spurious bias structure in the resulting similarity matrix, in particular when applied to fMRI data. This problem is especially severe when the signal-to-noise ratio is low and in cases where experimental conditions cannot be fully randomized in a task. We propose Bayesian Representational Similarity Analysis (BRSA), an alternative method for computing representational similarity, in which we treat the covariance structure of neural activity patterns as a hyper-parameter in a generative model of the neural data. By marginalizing over the unknown activity patterns, we can directly estimate this covariance structure from imaging data. This method offers significant reductions in bias and allows estimation of neural representational similarity with previously unattained levels of precision at low signal-to-noise ratio, without losing the possibility of deriving an interpretable distance measure from the estimated similarity. The method is closely related to Pattern Component Model (PCM), but instead of modeling the estimated neural patterns as in PCM, BRSA models the imaging data directly and is suited for analyzing data in which the order of task conditions is not fully counterbalanced. The probabilistic framework allows for jointly analyzing data from a group of participants. The method can also simultaneously estimate a signal-to-noise ratio map that shows where the learned representational structure is supported more strongly. Both this map and the learned covariance matrix can be used as a structured prior for maximum a posteriori estimation of neural activity patterns, which can be further used for fMRI decoding. Our method therefore paves the way towards a more unified and principled analysis of neural representations underlying fMRI signals. We make our tool freely available in Brain Imaging Analysis Kit (BrainIAK).
Radulescu, A., & Niv, Y. (2019). State representation in mental illness. Current Opinion in Neurobiology. PDFAbstract
Reinforcement learning theory provides a powerful set of computational ideas for modeling human learning and decision making. Reinforcement learning algorithms rely on state representations that enable efficient behavior by focusing only on aspects relevant to the task at hand. Forming such representations often requires selective attention to the sensory environment, and recalling memories of relevant past experiences. A striking range of psychiatric disorders, including bipolar disorder and schizophrenia, involve changes in these cognitive processes. We review and discuss evidence that these changes can be cast as altered state representation, with the goal of providing a useful transdiagnostic dimension along which mental disorders can be understood and compared.
Bennett, D., Silverstein, S. M., & Niv, Y. (2019). The two cultures of computational psychiatry. JAMA Psychiatry. PDFAbstract
Translating advances in neuroscience into benefits for patients with mental illness presents enormous challenges because it involves both the most complex organ, the brain, and its interaction with a similarly complex environment. Dealing with such complexities demands powerful techniques. Computational psychiatry combines multiple levels and types of computation with multiple types of data in an effort to improve understanding, prediction and treatment of mental illness. Computational psychiatry, broadly defined, encompasses two complementary approaches: data driven and theory driven. Data-driven approaches apply machine-learning methods to high-dimensional data to improve classification of disease, predict treatment outcomes or improve treatment selection. These approaches are generally agnostic as to the underlying mechanisms. Theory-driven approaches, in contrast, use models that instantiate prior knowledge of, or explicit hypotheses about, such mechanisms, possibly at multiple levels of analysis and abstraction. We review recent advances in both approaches, with an emphasis on clinical applications, and highlight the utility of combining them.
Langdon, A. J., Song, M., & Niv, Y. (2019). Uncovering the ‘state': Tracing the hidden state representations that structure learning and decision-making. Behavioural Processes , 167, 103891. PDFAbstract
We review the abstract concept of a ‘state' – an internal representation posited by reinforcement learning theories to be used by an agent, whether animal, human or artificial, to summarize the features of the external and internal environment that are relevant for future behavior on a particular task. Armed with this summary representation, an agent can make decisions and perform actions to interact effectively with the world. Here, we review recent findings from the neurobiological and behavioral literature to ask: ‘what is a state?' with respect to the internal representations that organize learning and decision making across a range of tasks. We find that state representations include information beyond a straightforward summary of the immediate cues in the environment, providing timing or contextual information from the recent or more distant past, which allows these additional factors to influence decision making and other goal-directed behaviors in complex and perhaps unexpected ways.
2018
Niv, Y. (2018). Deep down, you are a scientist. In Think tank: Forty neuroscientists explore the biological roots of human experience. PDFAbstract
You may not know it, but deep down you are a scientist. To be precise, your brain is a scientist—and a good one, too: the kind of scientist that makes clear hypotheses, gathers data from several sources, and then reaches a well-founded conclusion. Although we are not aware of the scientific experimentation occurring in our brain on a momentary basis, the scientific process is fundamental to how our brain works. This scientific process involves three key components. First: hypotheses. Our brain makes hypotheses, or predictions, all the time. The second component of good scientific work is gathering data—testing the hypothesis by comparing it to evidence. The neuroscientists gather data to test the theories about how the brain works from several sources—for example, behavior, invasive recordings of the activity of single cells in the brain, and noninvasive imaging of overall activity in large areas of the brain. Finally, after making precise, well-founded predictions and gathering data from all available sources, a scientist must interpret the empirical observations. It is important to realize that the perceived reality is subjective—it is interpreted—rather than an objective image of the world out there. And in some cases this interpretation can break down. For instance, in schizophrenia, meaningless events and distractors can take on outsized meaning in subjective interpretation, leading to hallucinations, delusions, and paranoia. Our memories are similarly a reflection of our own interpretations rather than a true record of events. (PsycINFO Database Record (c) 2018 APA, all rights reserved)
Rouhani, N., Norman, K. A., & Niv, Y. (2018). Dissociable effects of surprising rewards on learning and memory. Journal of Experimental Psychology: Learning Memory and Cognition , 44 (9), 1430–1443. PDFAbstract

Reward-prediction errors track the extent to which rewards deviate from expectations, and aid in learning. How do such errors in prediction interact with memory for the rewarding episode? Existing findings point to both cooperative and competitive interactions between learning and memory mechanisms. Here, we investigated whether learning about rewards in a high-risk context, with frequent, large prediction errors, would give rise to higher fidelity memory traces for rewarding events than learning in a low-risk context. Experiment 1 showed that recognition was better for items associated with larger absolute prediction errors during reward learning. Larger prediction errors also led to higher rates of learning about rewards. Interestingly we did not find a relationship between learning rate for reward and recognition-memory accuracy for items, suggesting that these two effects of prediction errors were caused by separate underlying mechanisms. In Experiment 2, we replicated these results with a longer task that posed stronger memory demands and allowed for more learning. We also showed improved source and sequence memory for items within the high-risk context. In Experiment 3, we controlled for the difficulty of reward learning in the risk environments, again replicating the previous results. Moreover, this control revealed that the high-risk context enhanced item-recognition memory beyond the effect of prediction errors. In summary, our results show that prediction errors boost both episodic item memory and incremental reward learning, but the two effects are likely mediated by distinct underlying systems.

Sharpe, M. J., Chang, C. Y., Liu, M. A., Batchelor, H. M., Mueller, L. E., Jones, J. L., Niv, Y., et al. (2018). Dopamine transients are sufficient and necessary for acquisition of model-based associations. Nature Neuroscience , 21 (10), 1493. PDFAbstract
Learning to predict reward is thought to be driven by dopaminergic prediction errors, which reflect discrepancies between actual and expected value. Here the authors show that learning to predict neutral events is also driven by prediction errors and that such value-neutral associative learning is also likely mediated by dopaminergic error signals.
Sharpe, M. J., Stalnaker, T. A., Schuck, N. W., Killcross, S., Schoenbaum, G., & Niv, Y. (2018). An Integrated Model of Action Selection: Distinct Modes of Cortical Control of Striatal Decision Making. Annual Review of Psychology. PDFAbstract
Making decisions in environments with few choice options is easy. We select the action that results in the most valued outcome. Making decisions in more complex environments, where the same action can produce different outcomes in different conditions, is much harder. In such circumstances, we propose that accurate action selection relies on top-down control from the prelimbic and orbitofrontal cortices over striatal activity through distinct thalamostriatal circuits. We suggest that the prelimbic cortex exerts direct influence over medium spiny neurons in the dorsomedial striatum to represent the state space relevant to the current environment. Conversely, the orbitofrontal cortex is argued to track a subject's position within that state space, likely through modulation of cholinergic interneurons.
Langdon, A. J., Sharpe, M. J., Schoenbaum, G., & Niv, Y. (2018). Model-based predictions for dopamine. Current Opinion in Neurobiology , 49, 1–7. PDFAbstract
Phasic dopamine responses are thought to encode a prediction-error signal consistent with model-free reinforcement learning theories. However, a number of recent findings highlight the influence of model-based computations on dopamine responses, and suggest that dopamine prediction errors reflect more dimensions of an expected outcome than scalar reward value. Here, we review a selection of these recent results and discuss the implications and complications of model-based predictions for computational theories of dopamine and learning.
Hermsdorff, G. B., Pereira, T., & Niv, Y. (2018). Quantifying Humans' Priors Over Graphical Representations of Tasks. In Springer Proceedings in Complexity (pp. 281–290). PDFAbstract
Schuck, N. W., Wilson, R. C., & Niv, Y. (2018). A State Representation for Reinforcement Learning and Decision-Making in the Orbitofrontal Cortex. In Goal-Directed Decision Making. PDFAbstract
Despite decades of research, the exact ways in which the orbitofrontal cortex (OFC) influences cognitive function have remained mysterious. Anatomically, the OFC is characterized by remarkably broad connectivity to sensory, limbic and subcortical areas, and functional studies have implicated the OFC in a plethora of functions ranging from facial processing to value-guided choice. Notwithstanding such diversity of findings, much research suggests that one important function of the OFC is to support decision making and reinforcement learning. Here, we describe a novel theory that posits that OFC's specific role in decision-making is to provide an up-to-date representation of task-related information, called a state representation. This representation reflects a mapping between distinct task states and sensory as well as unobservable information. We summarize evidence supporting the existence of such state representations in rodent and human OFC and argue that forming these state representations provides a crucial scaffold that allows animals to efficiently perform decision making and reinforcement learning in high-dimensional and partially observable environments. Finally, we argue that our theory offers an integrating framework for linking the diversity of functions ascribed to OFC and is in line with its wide ranging connectivity.
2017
Cohen, J. D., Daw, N. D., Engelhardt, B., Hasson, U., Li, K., Niv, Y., Norman, K. A., et al. (2017). Computational approaches to fMRI analysis. Nature Neuroscience , 20 (3), 304–313. PDFAbstract
Multi-walled carbon nanotubes (MWCNT) and carbon nanofibers (CNF) were created using chemical vapor deposition at growth temperatures between 500 and 750 C, which have increasing crystallinity with increasing growth temperature. We used Raman spectroscopy to analyze the samples. The intensity ratios compared to the G-band, and full-width at half-maximum, of all observable Raman bands in both the first and second-order region were investigated. Good match was observed for the defect related bands of the MWCNT samples and data found in the literature. Several second-order bands display a strong dependency to growth temperature. Similar growth temperature (and thus defect) dependencies were found between several first and second-order bands, which might aid in determining the physical causes of these bands. CNF show much weaker Raman features due to their low crystallinity, making them more difficult to analyse. The results of this work are used to give recommendations on how to investigate MWCNT and CNF crystallinity using Raman spectroscopy. Finally, we demonstrate that Raman spectroscopy can be used to distinguish between the MWCNT root and tip growth mechanism.
Gershman, S. J., Monfils, M. - H., Norman, K. A., & Niv, Y. (2017). The computational nature of memory modification. eLife , 6. PDFAbstract
Retrieving a memory can modify its influence on subsequent behavior. We develop a computational theory of memory modification, according to which modification of a memory trace occurs through classical associative learning, but which memory trace is eligible for modification depends on a structure learning mechanism that discovers the units of association by segmenting the stream of experience into statistically distinct clusters (latent causes). New memories are formed when the structure learning mechanism infers that a new latent cause underlies current sensory observations. By the same token, old memories are modified when old and new sensory observations are inferred to have been generated by the same latent cause. We derive this framework from probabilistic principles, and present a computational implementation. Simulations demonstrate that our model can reproduce the major experimental findings from studies of memory modification in the Pavlovian conditioning literature.
DuBrow, S., Rouhani, N., Niv, Y., & Norman, K. A. (2017). Does mental context drift or shift? Current Opinion in Behavioral Sciences , 17, 141–146. PDFAbstract
Theories of episodic memory have proposed that individual memory traces are linked together by a representation of context that drifts slowly over time. Recent data challenge the notion that contextual drift is always slow and passive. In particular, changes in one's external environment or internal model induce discontinuities in memory that are reflected in sudden changes in neural activity, suggesting that context can shift abruptly. Furthermore, context change effects are sensitive to top-down goals, suggesting that contextual drift may be an active process. These findings call for revising models of the role of context in memory, in order to account for abrupt contextual shifts and the controllable nature of context change.
Leong*, Y. C., Radulescu*, A., Daniel, R., DeWoskin, V., & Niv, Y. (2017). Dynamic Interaction between Reinforcement Learning and Attention in Multidimensional Environments. Neuron , 93 (2), 451–463. PDFAbstract
Little is known about the relationship between attention and learning during decision making. Using eye tracking and multivariate pattern analysis of fMRI data, we measured participants' dimensional attention as they performed a trial-and-error learning task in which only one of three stimulus dimensions was relevant for reward at any given time. Analysis of participants' choices revealed that attention biased both value computation during choice and value update during learning. Value signals in the ventromedial prefrontal cortex and prediction errors in the striatum were similarly biased by attention. In turn, participants' focus of attention was dynamically modulated by ongoing learning. Attentional switches across dimensions correlated with activity in a frontoparietal attention network, which showed enhanced connectivity with the ventromedial prefrontal cortex between switches. Our results suggest a bidirectional interaction between attention and learning: attention constrains learning to relevant dimensions of the environment, while we learn what to attend to via trial and error.
Sharpe, M. J., Marchant, N. J., Whitaker, L. R., Richie, C. T., Zhang, Y. J., Campbell, E. J., Koivula, P. P., et al. (2017). Lateral Hypothalamic GABAergic Neurons Encode Reward Predictions that Are Relayed to the Ventral Tegmental Area to Regulate Learning. Current Biology , 27 (14), 2089––2100.e5. PDFAbstract
Eating is a learned process. Our desires for specific foods arise through experience. Both electrical stimulation and optogenetic studies have shown that increased activity in the lateral hypothalamus (LH) promotes feeding. Current dogma is that these effects reflect a role for LH neurons in the control of the core motivation to feed, and their activity comes under control of forebrain regions to elicit learned food-motivated behaviors. However, these effects could also reflect the storage of associative information about the cues leading to food in LH itself. Here, we present data from several studies that are consistent with a role for LH in learning. In the first experiment, we use a novel GAD-Cre rat to show that optogenetic inhibition of LH $$\gamma$$-aminobutyric acid (GABA) neurons restricted to cue presentation disrupts the rats' ability to learn that a cue predicts food without affecting subsequent food consumption. In the second experiment, we show that this manipulation also disrupts the ability of a cue to promote food seeking after learning. Finally, we show that inhibition of the terminals of the LH GABA neurons in ventral-tegmental area (VTA) facilitates learning about reward-paired cues. These results suggest that the LH GABA neurons are critical for storing and later disseminating information about reward-predictive cues.
Auchter, A., Cormack, L. K., Niv, Y., Gonzalez-Lima, F., & Monfils, M. - H. (2017). Reconsolidation-Extinction Interactions in Fear Memory Attenuation: The Role of Inter-Trial Interval Variability. Frontiers in Behavioral Neuroscience , 11. PDFAbstract
Most of life is extinct, so incorporating some fossil evidence into analyses of macroevolution is typically seen as necessary to understand the diversification of life and patterns of morphological evolution. Here we test the effects of inclusion of fossils in a study of the body size evolution of afrotherian mammals, a clade that includes the elephants, sea cows and elephant shrews. We find that the inclusion of fossil tips has little impact on analyses of body mass evolution; from a small ancestral size (approx. 100 g), there is a shift in rate and an increase in mass leading to the larger-bodied Paenungulata and Tubulidentata, regardless of whether fossils are included or excluded from analyses. For Afrotheria, the inclusion of fossils and morphological character data affect phylogenetic topology, but these differences have little impact upon patterns of body mass evolution and these body mass evolutionary patterns are consistent with the fossil record. The largest differences between our analyses result from the evolutionary model, not the addition of fossils. For some clades, extant-only analyses may be reliable to reconstruct body mass evolution, but the addition of fossils and careful model selection is likely to increase confidence and accuracy of reconstructed macroevolutionary patterns.
2016
Eldar, E., Cohen, J. D., & Niv, Y. (2016). Amplified selectivity in cognitive processing implements the neural gain model of norepinephrine function. The Behavioral and brain sciences , 39, e206. PDFAbstract
Previous work has suggested that an interaction between local selective (e.g., glutamatergic) excitation and global gain modulation (via norepinephrine) amplifies selectivity in information processing. Mather et al. extend this existing theory by suggesting that localized gain modulation may further mediate this effect – an interesting prospect that invites new theoretical and experimental work.
Cai, M. B., & Schuck, N. W. (2016). A Bayesian method for reducing bias in neural representational similarity analysis. In D. D. Lee, U. V. Luxburg, I. Guyon, & R. Garnett (Ed.), Advances In Neural Information Processing Systems 29 (pp. 4952–4960) . Curran Associates, Inc. PDFAbstract
In neuroscience, the similarity matrix of neural activity patterns in response to different sensory stimuli or under different cognitive states reflects the structure of neural representational space. Existing methods derive point estimations of neural activity patterns from noisy neural imaging data, and the similarity is calculated from these point estimations. We show that this approach translates structured noise from estimated patterns into spurious bias structure in the resulting similarity matrix, which is especially severe when signal-to-noise ratio is low and experimental conditions cannot be fully randomized in a cognitive task. We propose an alternative Bayesian framework for computing representational similarity in which we treat the covariance structure of neural activity patterns as a hyperparameter in a generative model of the neural data, and directly estimate this covariance structure from imaging data while marginalizing over the unknown activity patterns. Converting the estimated covariance structure into a correlation matrix offers a much less biased estimate of neural representational similarity. Our method can also simultaneously estimate a signal-to-noise map that informs where the learned representational structure is supported more strongly, and the learned covariance matrix can be used as a structured prior to constrain Bayesian estimation of neural activity patterns. Our code is freely available in Brain Imaging Analysis Kit (Brainiak) (https://github.com/IntelPNI/brainiak).
Kurth-Nelson, Z., O'Doherty, J. P., Barch, D. M., Denève, S., Durstewitz, D., Frank, M. J., Gordon, J. A., et al. (2016). Computational Approaches for Studying Mechanisms of Psychiatric Disorders. In Computational Psychiatry . The MIT Press. PDFAbstract
Vast spectra of biological and psychological processes are potentially involved in the mechanisms of psychiatric illness. Computational neuroscience brings a diverse toolkit to bear on understanding these processes. This chapter begins by organizing the many ways in which computational neuroscience may provide insight to the mechanisms of psychiatric illness. It then contextualizes the quest for deep mechanistic understanding through the perspective that even partial or nonmechanistic understanding can be applied productively. Finally, it questions the standards by which these approaches...
Eldar, E., Niv, Y., & Cohen, J. D. (2016). Do You See the Forest or the Tree? Neural Gain and Breadth Versus Focus in Perceptual Processing. Psychological Science , 27 (12), 1632–1643. PDFAbstract
When perceiving rich sensory information, some people may integrate its various aspects, whereas other people may selectively focus on its most salient aspects. We propose that neural gain modulates the trade-off between breadth and selectivity, such that high gain focuses perception on those aspects of the information that have the strongest, most immediate influence, whereas low gain allows broader integration of different aspects. We illustrate our hypothesis using a neural-network model of ambiguous-letter perception. We then report an experiment demonstrating that, as predicted by the model, pupil-diameter indices of higher gain are associated with letter perception that is more selectively focused on the letter's shape or, if primed, its semantic content. Finally, we report a recognition-memory experiment showing that the relationship between gain and selective processing also applies when the influence of different stimulus features is voluntarily modulated by task demands.
Arkadir, D., Radulescu, A., Raymond, D., Lubarr, N., Bressman, S. B., Mazzoni, P., & Niv, Y. (2016). DYT1 dystonia increases risk taking in humans. eLife , 5 (JUN2016). PDFAbstract
It has been difficult to link synaptic modification to overt behavioral changes. Rodent models of DYT1 dystonia, a motor disorder caused by a single gene mutation, demonstrate increased long-term potentiation and decreased long-term depression in corticostriatal synapses. Computationally, such asymmetric learning predicts risk taking in probabilistic tasks. Here we demonstrate abnormal risk taking in DYT1 dystonia patients, which is correlated with disease severity, thereby supporting striatal plasticity in shaping choice behavior in humans.
Radulescu, A., Daniel, R., & Niv, Y. (2016). The effects of aging on the interaction between reinforcement learning and attention. Psychology and Aging , 31 (7), 747–757. PDFAbstract
Predicting the binding mode of flexible polypeptides to proteins is an important task that falls outside the domain of applicability of most small molecule and protein−protein docking tools. Here, we test the small molecule flexible ligand docking program Glide on a set of 19 non-$$\alpha$$-helical peptides and systematically improve pose prediction accuracy by enhancing Glide sampling for flexible polypeptides. In addition, scoring of the poses was improved by post-processing with physics-based implicit solvent MM- GBSA calculations. Using the best RMSD among the top 10 scoring poses as a metric, the success rate (RMSD ≤ 2.0 \AAfor the interface backbone atoms) increased from 21% with default Glide SP settings to 58% with the enhanced peptide sampling and scoring protocol in the case of redocking to the native protein structure. This approaches the accuracy of the recently developed Rosetta FlexPepDock method (63% success for these 19 peptides) while being over 100 times faster. Cross-docking was performed for a subset of cases where an unbound receptor structure was available, and in that case, 40% of peptides were docked successfully. We analyze the results and find that the optimized polypeptide protocol is most accurate for extended peptides of limited size and number of formal charges, defining a domain of applicability for this approach.
Schuck, N. W., Cai, M. B., Wilson, R. C., & Niv, Y. (2016). Human Orbitofrontal Cortex Represents a Cognitive Map of State Space. Neuron , 91 (6), 1402–1412. PDFAbstract
Although the orbitofrontal cortex (OFC) has been studied intensely for decades, its precise functions have remained elusive. We recently hypothesized that the OFC contains a “cognitive map” of task space in which the current state of the task is represented, and this representation is especially critical for behavior when states are unobservable from sensory input. To test this idea, we apply pattern-classification techniques to neuroimaging data from humans performing a decision-making task with 16 states. We show that unobservable task states can be decoded from activity in OFC, and decoding accuracy is related to task performance and the occurrence of individual behavioral errors. Moreover, similarity between the neural representations of consecutive states correlates with behavioral accuracy in corresponding state transitions. These results support the idea that OFC represents a cognitive map of task space and establish the feasibility of decoding state representations in humans using non-invasive neuroimaging.
Eldar*, E., Rutledge*, R. B., Dolan, R. J., & Niv, Y. (2016). Mood as Representation of Momentum. Trends in Cognitive Sciences , 20 (1), 15–24. PDFAbstract
Experiences affect mood, which in turn affects subsequent experiences. Recent studies suggest two specific principles. First, mood depends on how recent reward outcomes differ from expectations. Second, mood biases the way we perceive outcomes (e.g., rewards), and this bias affects learning about those outcomes. We propose that this two-way interaction serves to mitigate inefficiencies in the application of reinforcement learning to real-world problems. Specifically, we propose that mood represents the overall momentum of recent outcomes, and its biasing influence on the perception of outcomes 'corrects' learning to account for environmental dependencies. We describe potential dysfunctions of this adaptive mechanism that might contribute to the symptoms of mood disorders.
Chan, S. C. Y., Niv*, Y., & Norman*, K. A. (2016). A probability distribution over latent causes, in the orbitofrontal cortex. Journal of Neuroscience , 36 (30), 7817–7828. PDFAbstract
The orbitofrontal cortex (OFC) has been implicated in both the representation of "state," in studies of reinforcement learning and decision making, and also in the representation of "schemas," in studies of episodic memory. Both of these cognitive constructs require a similar inference about the underlying situation or "latent cause" that generates our observations at any given time. The statistically optimal solution to this inference problem is to use Bayes' rule to compute a posterior probability distribution over latent causes. To test whether such a posterior probability distribution is represented in the OFC, we tasked human participants with inferring a probability distribution over four possible latent causes, based on their observations. Using fMRI pattern similarity analyses, we found that BOLD activity in the OFC is best explained as representing the (log-transformed) posterior distribution over latent causes. Furthermore, this pattern explained OFC activity better than other task-relevant alternatives, such as the most probable latent cause, the most recent observation, or the uncertainty over latent causes. ©2016 the authors.
Niv, Y., & Langdon, A. J. (2016). Reinforcement learning with Marr. Current Opinion in Behavioral Sciences , 11, 67–73. PDFAbstract
To many, the poster child for David Marr's famous three levels of scientific inquiry is reinforcement learning – a computational theory of reward optimization, which readily prescribes algorithmic solutions that evidence striking resemblance to signals found in the brain, suggesting a straightforward neural implementation. Here we review questions that remain open at each level of analysis, concluding that the path forward to their resolution calls for inspiration across levels, rather than a focus on mutual constraints.
Takahashi*, Y. K., Langdon*, A. J., Niv, Y., & Schoenbaum, G. (2016). Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum. Neuron , 91 (1), 182–193. PDFAbstract
Dopamine neurons signal reward prediction errors. This requires accurate reward predictions. It has been suggested that the ventral striatum provides these predictions. Here we tested this hypothesis by recording from putative dopamine neurons in the VTA of rats performing a task in which prediction errors were induced by shifting reward timing or number. In controls, the neurons exhibited error signals in response to both manipulations. However, dopamine neurons in rats with ipsilateral ventral striatal lesions exhibited errors only to changes in number and failed to respond to changes in timing of reward. These results, supported by computational modeling, indicate that predictions about the temporal specificity and the number of expected reward are dissociable and that dopaminergic prediction-error signals rely on the ventral striatum for the former but not the latter.
2015
Gershman, S. J., Norman, K. A., & Niv, Y. (2015). Discovering latent causes in reinforcement learning. Current Opinion in Behavioral Sciences , 5 43–50. PDFAbstract
Effective reinforcement learning hinges on having an appropriate state representation. But where does this representation come from? We argue that the brain discovers state representations by trying to infer the latent causal structure of the task at hand, and assigning each latent cause to a separate state. In this paper, we review several implications of this latent cause framework, with a focus on Pavlovian conditioning. The framework suggests that conditioning is not the acquisition of associations between cues and outcomes, but rather the acquisition of associations between latent causes and observable stimuli. A latent cause interpretation of conditioning enables us to begin answering questions that have frustrated classical theories: Why do extinguished responses sometimes return? Why do stimuli presented in compound sometimes summate and sometimes do not? Beyond conditioning, the principles of latent causal inference may provide a general theory of structure learning across cognitive domains.
Niv, Y., Langdon, A. J., & Radulescu, A. (2015). A free-choice premium in the basal ganglia. Trends in Cognitive Sciences , 19 (1), 4–5. PDFAbstract
Apparently, the act of free choice confers value: when selecting between an item that you had previously chosen and an identical item that you had been forced to take, the former is often preferred. What could be the neural underpinnings of this free-choice bias in decision making? An elegant study recently published in Neuron suggests that enhanced reward learning in the basal ganglia may be the culprit.
Daniel, R., Schuck, N. W., & Niv, Y. (2015). How to divide and conquer the world, one step at a time. Proceedings of the National Academy of Sciences , 112 (10), 2929–2930. PDF
Eldar, E., & Niv, Y. (2015). Interaction between emotional state and learning underlies mood instability. Nature Communications , 6 (1), 6149. PDFAbstract
Intuitively, good and bad outcomes affect our emotional state, but whether the emotional state feeds back onto the perception of outcomes remains unknown. Here, we use behaviour and functional neuroimaging of human participants to investigate this bidirectional interaction, by comparing the evaluation of slot machines played before and after an emotion-impacting wheel-of-fortune draw. Results indicate that self-reported mood instability is associated with a positive-feedback effect of emotional state on the perception of outcomes. We then use theoretical simulations to demonstrate that such positive feedback would result in mood destabilization. Taken together, our results suggest that the interaction between emotional state and learning may play a significant role in the emergence of mood instability.
Wilson, R. C., & Niv, Y. (2015). Is Model Fitting Necessary for Model-Based fMRI? PLoS Comput Biol , 11 (6), e1004237. PDFAbstract
Model-based analysis of fMRI data is an important tool for investigating the computational role of different brain regions. With this method, theoretical models of behavior can be leveraged to find the brain structures underlying variables from specific algorithms, such as prediction errors in reinforcement learning. One potential weakness with this approach is that models often have free parameters and thus the results of the analysis may depend on how these free parameters are set. In this work we asked whether this hypothetical weakness is a problem in practice. We first developed general closed-form expressions for the relationship between results of fMRI analyses using different regressors, e.g., one corresponding to the true process underlying the measured data and one a model-derived approximation of the true generative regressor. Then, as a specific test case, we examined the sensitivity of model-based fMRI to the learning rate parameter in reinforcement learning, both in theory and in two previously-published datasets. We found that even gross errors in the learning rate lead to only minute changes in the neural results. Our findings thus suggest that precise model fitting is not always necessary for model-based fMRI. They also highlight the difficulty in using fMRI data for arbitrating between different models or model parameters. While these specific results pertain only to the effect of learning rate in simple reinforcement learning models, we provide a template for testing for effects of different parameters in other models.
Gershman, S. J., & Niv, Y. (2015). Novelty and Inductive Generalization in Human Reinforcement Learning. Topics in Cognitive Science , 7 (3), 391–415. PDFAbstract
In reinforcement learning (RL), a decision maker searching for the most rewarding option is often faced with the question: What is the value of an option that has never been tried before? One way to frame this question is as an inductive problem: How can I generalize my previous experi-ence with one set of options to a novel option? We show how hierarchical Bayesian inference can be used to solve this problem, and we describe an equivalence between the Bayesian model and temporal difference learning algorithms that have been proposed as models of RL in humans and animals. According to our view, the search for the best option is guided by abstract knowledge about the relationships between different options in an environment, resulting in greater search effi-ciency compared to traditional RL algorithms previously applied to human cognition. In two behav-ioral experiments, we test several predictions of our model, providing evidence that humans learn and exploit structured inductive knowledge to make predictions about novel options. In light of this model, we suggest a new interpretation of dopaminergic responses to novelty.
Niv, Y., Daniel, R., Geana, A., Gershman, S. J., Leong, Y. C., Radulescu, A., & Wilson, R. C. (2015). Reinforcement Learning in Multidimensional Environments Relies on Attention Mechanisms. Journal of Neuroscience , 35 (21), 8145–8157. PDFAbstract
In recent years, ideas from the computational field of reinforcement learning have revolutionized the study of learning in the brain, famously providing new, precise theories of how dopamine affects learning in the basal ganglia. However, reinforcement learning algorithms are notorious for not scaling well to multidimensional environments, as is required for real-world learning. We hypothesized that the brain naturally reduces the dimensionality of real-world problems to only those dimensions that are relevant to predicting reward, and conducted an experiment to assess by what algorithms and with what neural mechanisms this "representation learning" process is realized in humans. Our results suggest that a bilateral attentional control network comprising the intraparietal sulcus, precuneus, and dorsolateral prefrontal cortex is involved in selecting what dimensions are relevant to the task at hand, effectively updating the task representation through trial and error. In this way, cortical attention mechanisms interact with learning in the basal ganglia to solve the "curse of dimensionality" in reinforcement learning.
Dunsmoor, J. E., Niv, Y., Daw, N. D., & Phelps, E. A. (2015). Rethinking Extinction. Neuron , 88 (1), 47–63. PDFAbstract
Extinction serves as the leading theoretical framework and experimental model to describe how learned behaviors diminish through absence of anticipated reinforcement. In the past decade, extinction has moved beyond the realm of associative learning theory and behavioral experimentation in animals and has become a topic of considerable interest in the neuroscience of learning, memory, and emotion. Here, we review research and theories of extinction, both as a learning process and as a behavioral technique, and consider whether traditional understandings warrant a re-examination. We discuss the neurobiology, cognitive factors, and major computational theories, and revisit the predominant view that extinction results in new learning that interferes with expression of the original memory. Additionally, we reconsider the limitations of extinction as a technique to prevent the relapse of maladaptive behavior and discuss novel approaches, informed by contemporary theoretical advances, that augment traditional extinction methods to target and potentially alter maladaptive memories.
Sharpe, M. J., Wikenheiser, A. M., Niv, Y., & Schoenbaum, G. (2015). The State of the Orbitofrontal Cortex. Neuron , 88 (6), 1075–1077. PDFAbstract
State representation is fundamental to behavior. However, identifying the true state of the world is challenging when explicit cues are ambiguous. Here, Bradfield and colleagues show that the medial OFC is critical for using associative information to discriminate ambiguous states. State representation is fundamental to behavior. However, identifying the true state of the world is challenging when explicit cues are ambiguous. Here, Bradfield and colleagues show that the medial OFC is critical for using associative information to discriminate ambiguous states.
2014
Geana, A., & Niv, Y. (2014). Causal model comparison shows that human representation learning is not Bayesian. Cold Spring Harbor Symposia on Quantitative Biology , 79, 161–168. PDFAbstract
How do we learn what features of our multidimensional environment are relevant in a given task? To study the computational process underlying this type of "representation learning," we propose a novel method of causal model comparison. Participants played a probabilistic learning task that required them to identify one relevant feature among several irrelevant ones. To compare between two models of this learning process, we ran each model alongside the participant during task performance, making predictions regarding the values underlying the participant's choices in real time. To test the validity of each model's predictions, we used the predicted values to try to perturb the participant's learning process: We crafted stimuli to either facilitate or hinder comparison between the most highly valued features. A model whose predictions coincide with the learned values in the participant's mind is expected to be effective in perturbing learning in this way, whereas a model whose predictions stray from the true learning process should not. Indeed, we show that in our task a reinforcement-learning model could help or hurt participants' learning, whereas a Bayesian ideal observer model could not. Beyond informing us about the notably suboptimal (but computationally more tractable) substrates of human representation learning, our manipulation suggests a sensitive method for model comparison, which allows us to change the course of people's learning in real time.
Soto, F. A., Gershman, S. J., & Niv, Y. (2014). Explaining compound generalization in associative and causal learning through rational principles of dimensional generalization. Psychological Review , 121 (3), 526–558. PDFAbstract
How do we apply learning from one situation to a similar, but not identical, situation? The principles governing the extent to which animals and humans generalize what they have learned about certain stimuli to novel compounds containing those stimuli vary depending on a number of factors. Perhaps the best studied among these factors is the type of stimuli used to generate compounds. One prominent hypothesis is that different generalization principles apply depending on whether the stimuli in a compound are similar or dissimilar to each other. However, the results of many experiments cannot be explained by this hypothesis. Here, we propose a rational Bayesian theory of compound generalization that uses the notion of consequential regions, first developed in the context of rational theories of multidimensional generalization, to explain the effects of stimulus factors on compound generalization. The model explains a large number of results from the compound generalization literature, including the influence of stimulus modality and spatial contiguity on the summation effect, the lack of influence of stimulus factors on summation with a recovered inhibitor, the effect of spatial position of stimuli on the blocking effect, the asymmetrical generalization decrement in overshadowing and external inhibition, and the conditions leading to a reliable external inhibition effect. By integrating rational theories of compound and dimensional generalization, our model provides the first comprehensive computational account of the effects of stimulus factors on compound generalization, including spatial and temporal contiguity between components, which have posed long-standing problems for rational theories of associative and causal learning.
Solway*, A., Diuk*, C., Córdova, N., Yee, D., Barto, A. G., Niv, Y., & Botvinick, M. M. (2014). Optimal Behavioral Hierarchy. PLoS Computational Biology , 10 (8), e1003779. PDFAbstract
Human behavior has long been recognized to display hierarchical structure: actions fit together into subtasks, which cohere into extended goal-directed activities. Arranging actions hierarchically has well established benefits, allowing behaviors to be represented efficiently by the brain, and allowing solutions to new tasks to be discovered easily. However, these payoffs depend on the particular way in which actions are organized into a hierarchy, the specific way in which tasks are carved up into subtasks. We provide a mathematical account for what makes some hierarchies better than others, an account that allows an optimal hierarchy to be identified for any set of tasks. We then present results from four behavioral experiments, suggesting that human learners spontaneously discover optimal action hierarchies.
Wilson, R. C., Takahashi, Y. K., Schoenbaum, G., & Niv, Y. (2014). Orbitofrontal Cortex as a Cognitive Map of Task Space. D. D. Lee, U. V. Luxburg, I. Guyon, & R. Garnett (Ed.), Neuron , 81 (2), 267–279 . Salt Lake City, Utah, Elsevier Inc. PDFAbstract
Orbitofrontal cortex (OFC) has long been known to play an important role in decision making. However, the exact nature of that role has remained elusive. Here, we propose a unifying theory of OFC function. We hypothesize that OFC provides an abstraction of currently available information in the form of a labeling of the current task state, which is used for reinforcement learning (RL) elsewhere in the brain. This function is especially critical when task states include unobservable information, for instance, from working memory. We use this framework to explain classic findings in reversal learning, delayed alternation, extinction, and devaluation as well as more recent findings showing the effect of OFC lesions on the firing of dopaminergic neurons in ventral tegmental area (VTA) in rodents performing an RL task. In addition, we generate a number of testable experimental predictions that can distinguish our theory from other accounts of OFC function. ?? 2014 Elsevier Inc.
Gershman, S. J., Radulescu, A., Norman, K. A., & Niv, Y. (2014). Statistical Computations Underlying the Dynamics of Memory Updating. PLoS Computational Biology , 10 (11), e1003939. PDFAbstract
Psychophysical and neurophysiological studies have suggested that memory is not simply a carbon copy of our experience: Memories are modified or new memories are formed depending on the dynamic structure of our experience, and specifically, on how gradually or abruptly the world changes. We present a statistical theory of memory formation in a dynamic environment, based on a nonparametric generalization of the switching Kalman filter. We show that this theory can qualitatively account for several psychophysical and neural phenomena, and present results of a new visual memory experiment aimed at testing the theory directly. Our experimental findings suggest that humans can use temporal discontinuities in the structure of the environment to determine when to form new memory traces. The statistical perspective we offer provides a coherent account of the conditions under which new experience is integrated into an old memory versus forming a new memory, and shows that memory formation depends on inferences about the underlying structure of our experience.
2013
Diuk, C., Schapiro, A., Córdova, N., Ribas-Fernandes, J. J. F., Niv, Y., & Botvinick, M. M. (2013). Divide and conquer: Hierarchical reinforcement learning and task decomposition in humans. Computational and Robotic Models of the Hierarchical Organization of Behavior (Vol. 9783642398, pp. 271–291). PDFAbstract
The field of computational reinforcement learning (RL) has proved extremely useful in research on human and animal behavior and brain function. However, the simple forms of RL considered in most empirical research do not scale well, making their relevance to complex, real-world behavior unclear. In computational RL, one strategy for addressing the scaling problem is to intro-duce hierarchical structure, an approach that has intriguing parallels with human behavior. We have begun to investigate the potential relevance of hierarchical RL (HRL) to human and animal behavior and brain function. In the present chapter, we first review two results that show the existence of neural correlates to key predictions from HRL. Then, we focus on one aspect of this work, which deals with the question of how action hierarchies are initially established. Work in HRL suggests that hierarchy learning is accomplished by identifying useful subgoal states, and that this might in turn be accomplished through a structural analysis of the given task domain. We review results from a set of behavioral and neuroimaging experiments, in which we have investigated the relevance of these ideas to human learning and decision making.
Eldar, E., Cohen, J. D., & Niv, Y. (2013). The effects of neural gain on attention and learning. Nature Neuroscience , 16 (8), 1146–1153. PDFAbstract
Attention is commonly thought to be manifest through local variations in neural gain. However, what would be the effects of brain-wide changes in gain? We hypothesized that global fluctuations in gain modulate the breadth of attention and the degree to which processing is focused on aspects of the environment to which one is predisposed to attend. We found that measures of pupil diameter, which are thought to track levels of locus coeruleus norepinephrine activity and neural gain, were correlated with the degree to which learning was focused on stimulus dimensions that individual human participants were more predisposed to process. In support of our interpretation of this effect in terms of global changes in gain, we found that the measured pupillary and behavioral variables were strongly correlated with global changes in the strength and clustering of functional connectivity, as brain-wide fluctuations of gain would predict.
Gershman, S. J., Jones, C. E., Norman, K. A., Monfils, M. - H., & Niv, Y. (2013). Gradual extinction prevents the return of fear: implications for the discovery of state. Front Behav Neurosci , 7 164. CorrigendumAbstract

Fear memories are notoriously difficult to erase, often recovering over time. The longstanding explanation for this finding is that, in extinction training, a new memory is formed that competes with the old one for expression but does not otherwise modify it. This explanation is at odds with traditional models of learning such as Rescorla-Wagner and reinforcement learning. A possible reconciliation that was recently suggested is that extinction training leads to the inference of a new state that is different from the state that was in effect in the original training. This solution, however, raises a new question: under what conditions are new states, or new memories formed? Theoretical accounts implicate persistent large prediction errors in this process. As a test of this idea, we reasoned that careful design of the reinforcement schedule during extinction training could reduce these prediction errors enough to prevent the formation of a new memory, while still decreasing reinforcement sufficiently to drive modification of the old fear memory. In two Pavlovian fear-conditioning experiments, we show that gradually reducing the frequency of aversive stimuli, rather than eliminating them abruptly, prevents the recovery of fear. This finding has important implications for theories of state discovery in reinforcement learning.

Diuk, C., Tsai, K., Wallis, J., Botvinick, M. M., & Niv, Y. (2013). Hierarchical Learning Induces Two Simultaneous, But Separable, Prediction Errors in Human Basal Ganglia. Journal of Neuroscience , 33 (13), 5797–5805. PDFAbstract
Studies suggest that dopaminergic neurons report a unitary, global reward prediction error signal. However, learning in complex real-life tasks, in particular tasks that show hierarchical structure, requires multiple prediction errors that may coincide in time. We used functional neuroimaging to measure prediction error signals in humans performing such a hierarchical task involving simultaneous, uncorrelated prediction errors. Analysis of signals in a priori anatomical regions of interest in the ventral striatum and the ventral tegmental area indeed evidenced two simultaneous, but separable, prediction error signals corresponding to the two levels of hierarchy in the task. This result suggests that suitably designed tasks may reveal a more intricate pattern of firing in dopaminergic neurons. Moreover, the need for downstream separation of these signals implies possible limitations on the number of different task levels that we can learn about simultaneously.
Schoenbaum, G., Stalnaker, T. A., & Niv, Y. (2013). How Did the Chicken Cross the Road? With Her Striatal Cholinergic Interneurons, Of Course. Neuron , 79 (1), 3–6. PDFAbstract
Recognizing when the world changes is fundamental for normal learning. In this issue of Neuron, Bradfield etal. (2013) show that cholinergic interneurons in dorsomedial striatum are critical to the process whereby new states of the world are appropriately registered and retrieved during associative learning
Niv, Y. (2013). Neuroscience: Dopamine ramps up. Nature , 500 (7464), 533–535. PDFAbstract
We thought we had figured out dopamine, a neuromodulator involved in everything from learning to addiction. But the finding that dopamine levels ramp up as rats navigate to a reward may overthrow current theories. See Letter p.575
Gershman, S. J., & Niv, Y. (2013). Perceptual estimation obeys Occam's razor. Frontiers in Psychology , 4 (SEP), 623. PDFAbstract
Theoretical models of unsupervised category learning postulate that humans “invent” categories to accommodate new patterns, but tend to group stimuli into a small number of categories. This “Occam's razor” principle is motivated by normative rules of statistical inference. If categories influence perception, then one should find effects of category invention on simple perceptual estimation. In a series of experiments, we tested this prediction by asking participants to estimate the number of colored circles on a computer screen, with the number of circles drawn from a color-specific distribution. When the distributions associated with each color overlapped substantially, participants' estimates were biased toward values intermediate between the two means, indicating that subjects ignored the color of the circles and grouped different-colored stimuli into one perceptual category. These data suggest that humans favor simpler explanations of sensory inputs. In contrast, when the distributions associated with each color overlapped minimally, the bias was reduced (i.e., the estimates for each color were closer to the true means), indicating that sensory evidence for more complex explanations can override the simplicity bias. We present a rational analysis of our task, showing how these qualitative patterns can arise from Bayesian computations.
2012
Gershman, S. J., & Niv, Y. (2012). Exploring a latent cause theory of classical conditioning. Learn Behav , 40 (3), 255–268. PDFAbstract
We frame behavior in classical conditioning experiments as the product of normative statistical inference. According to this theory, animals learn an internal model of their environment from experience. The basic building blocks of this internal model are latent causes-explanatory constructs inferred by the animal that partition observations into coherent clusters. Generalization of conditioned responding from one cue to another arises from the animal's inference that the cues were generated by the same latent cause. Through a wide range of simulations, we demonstrate where the theory succeeds and where it fails as a general account of classical conditioning.
Lucantonio, F., Stalnaker, T. A., Shaham, Y., Niv, Y., & Schoenbaum, G. (2012). The impact of orbitofrontal dysfunction on cocaine addiction. Nature Neuroscience , 15 (3), 358–366. PDFAbstract
Cocaine addiction is characterized by poor judgment and maladaptive decision-making. Here we review evidence implicating the orbitofrontal cortex in such behavior. This evidence suggests that cocaine-induced changes in orbitofrontal cortex disrupt the representation of states and transition functions that form the basis of flexible and adaptive 'model-based' behavioral control. By impairing this function, cocaine exposure leads to an overemphasis on less flexible, maladaptive 'model-free' control systems. We propose that such an effect accounts for the complex pattern of maladaptive behaviors associated with cocaine addiction.
Wilson, R. C., & Niv, Y. (2012). Inferring Relevance in a Changing World. Frontiers in Human Neuroscience , 5 (JANUARY 2012), 189. PDFAbstract
Reinforcement learning models of human and animal learning usually concentrate on how we learn the relationship between different stimuli or actions and rewards. However, in real-world situations "stimuli" are ill-defined. On the one hand, our immediate environment is extremely multidimensional. On the other hand, in every decision making scenario only a few aspects of the environment are relevant for obtaining reward, while most are irrelevant. Thus a key question is how do we learn these relevant dimensions, that is, how do we learn what to learn about? We investigated this process of "representation learning" experimentally, using a task in which one stimulus dimension was relevant for determining reward at each point in time. As in real life situations, in our task the relevant dimension can change without warning, adding ever-present uncertainty engendered by a constantly changing environment. We show that human performance on this task is better described by a suboptimal strategy based on selective attention and serial-hypothesis-testing rather than a normative strategy based on probabilistic inference. From this, we conjecture that the problem of inferring relevance in general scenarios is too computationally demanding for the brain to solve optimally. As a result the brain utilizes approximations, employing these even in simplified scenarios in which optimal representation learning is tractable, such as the one in our experiment.
Niv, Y., Edlund, J. A., Dayan, P. D., & O'Doherty, J. P. (2012). Neural Prediction Errors Reveal a Risk-Sensitive Reinforcement-Learning Process in the Human Brain. Journal of Neuroscience , 32 (2), 551–562. PDFAbstract
Humans and animals are exquisitely, though idiosyncratically, sensitive to risk or variance in the outcomes of their actions. Economic, psychological, and neural aspects of this are well studied when information about risk is provided explicitly. However, we must normally learn about outcomes from experience, through trial and error. Traditional models of such reinforcement learning focus on learning about the mean reward value of cues and ignore higher order moments such as variance. We used fMRI to test whether the neural correlates of human reinforcement learning are sensitive to experienced risk. Our analysis focused on anatomically delineated regions of a priori interest in the nucleus accumbens, where blood oxygenation level-dependent (BOLD) signals have been suggested as correlating with quantities derived from reinforcement learning. We first provide unbiased evidence that the raw BOLD signal in these regions corresponds closely to a reward prediction error. We then derive from this signal the learned values of cues that predict rewards of equal mean but different variance and show that these values are indeed modulated by experienced risk. Moreover, a close neurometric-psychometric coupling exists between the fluctuations of the experience-based evaluations of risky options that we measured neurally and the fluctuations in behavioral risk aversion. This suggests that risk sensitivity is integral to human learning, illuminating economic models of choice, neuroscientific models of affective learning, and the workings of the underlying neural mechanisms.
2011
Niv, Y., & Chan, S. (2011). On the value of information and other rewards. Nature Neuroscience , 14 (9), 1095–1097. PDFAbstract
Knowledge is not just power. Even if advance information can not influence an upcoming event, people (and animals) prefer to know ahead of time what the outcome will be. According to the firing patterns of neurons in the lateral habenula, from the brain's perspective, knowledge is also water—or at least its equivalent in terms of reward.
Takahashi, Y. K., Roesch, M. R., Wilson, R. C., Toreson, K., O'Donnell, P., Niv, Y., & Schoenbaum, G. (2011). Expectancy-related changes in firing of dopamine neurons depend on orbitofrontal cortex. Nature Neuroscience , 14 (12), 1590–1597. PDFAbstract
The orbitofrontal cortex has been hypothesized to carry information regarding the value of expected rewards. Such information is essential for associative learning, which relies on comparisons between expected and obtained reward for generating instructive error signals. These error signals are thought to be conveyed by dopamine neurons. To test whether orbitofrontal cortex contributes to these error signals, we recorded from dopamine neurons in orbitofrontal-lesioned rats performing a reward learning task. Lesions caused marked changes in dopaminergic error signaling. However, the effect of lesions was not consistent with a simple loss of information regarding expected value. Instead, without orbitofrontal input, dopaminergic error signals failed to reflect internal information about the impending response that distinguished externally similar states leading to differently valued future rewards. These results are consistent with current conceptualizations of orbitofrontal cortex as supporting model-based behavior and suggest an unexpected role for this information in dopaminergic error signaling.
Eldar, E., Morris, G., & Niv, Y. (2011). The effects of motivation on response rate: A hidden semi-Markov model analysis of behavioral dynamics. Journal of Neuroscience Methods , 201 (1), 251–261. PDFAbstract
A central goal of neuroscience is to understand how neural dynamics bring about the dynamics of behavior. However, neural and behavioral measures are noisy, requiring averaging over trials and subjects. Unfortunately, averaging can obscure the very dynamics that we are interested in, masking abrupt changes and artificially creating gradual processes. We develop a hidden semi-Markov model for precisely characterizing dynamic processes and their alteration due to experimental manipulations. This method takes advantage of multiple trials and subjects without compromising the information available in individual events within a trial. We apply our model to studying the effects of motivation on response rates, analyzing data from hungry and sated rats trained to press a lever to obtain food rewards on a free-operant schedule. Our method can accurately account for punctate changes in the rate of responding and for sequential dependencies between responses. It is ideal for inferring the statistics of underlying response rates and the probability of switching from one response rate to another. Using the model, we show that hungry rats have more distinct behavioral states that are characterized by high rates of responding and they spend more time in these high-press-rate states. Moreover, hungry rats spend less time in, and have fewer distinct states that are characterized by a lack of responding (Waiting/Eating states). These results demonstrate the utility of our analysis method, and provide a precise quantification of the effects of motivation on response rates. ©2011 Elsevier B.V.
Ribas-Fernandes, J. J. F., Solway, A., Diuk, C., McGuire, J. T., Barto, A. G., Niv, Y., & Botvinick, M. M. (2011). A neural signature of hierarchical reinforcement learning. Neuron , 71 (2), 370–379. PDFAbstract
Human behavior displays hierarchical structure: simple actions cohere into subtask sequences, which work together to accomplish overall task goals. Although the neural substrates of such hierarchy have been the target of increasing research, they remain poorly understood. We propose that the computations supporting hierarchical behavior may relate to those in hierarchical reinforcement learning (HRL), a machine-learning framework that extends reinforcement-learning mechanisms into hierarchical domains. To test this, we leveraged a distinctive prediction arising from HRL. In ordinary reinforcement learning, reward prediction errors are computed when there is an unanticipated change in the prospects for accomplishing overall task goals. HRL entails that prediction errors should also occur in relation to task subgoals. In three neuroimaging studies we observed neural responses consistent with such subgoal-related reward prediction errors, within structures previously implicated in reinforcement learning. The results reported support the relevance of HRL to the neural processes underlying hierarchical behavior.
McDannald, M. A., Lucantonio, F., Burke, K. A., Niv, Y., & Schoenbaum, G. (2011). Ventral Striatum and Orbitofrontal Cortex Are Both Required for Model-Based, But Not Model-Free, Reinforcement Learning. Journal of Neuroscience , 31 (7), 2700–2705. PDFAbstract
In many cases, learning is thought to be driven by differences between the value of rewards we expect and rewards we actually receive. Yet learning can also occur when the identity of the reward we receive is not as expected, even if its value remains unchanged. Learning from changes in reward identity implies access to an internal model of the environment, from which information about the identity of the expected reward can be derived. As a result, such learning is not easily accounted for by model-free reinforcement learning theories such as temporal difference reinforcement learning (TDRL), which predicate learning on changes in reward value, but not identity. Here, we used unblocking procedures to assess learning driven by value- versus identity-based prediction errors. Rats were trained to associate distinct visual cues with different food quantities and identities. These cues were subsequently presented in compound with novel auditory cues and the reward quantity or identity was selectively changed. Unblocking was assessed by presenting the auditory cues alone in a probe test. Consistent with neural implementations of TDRL models, we found that the ventral striatum was necessary for learning in response to changes in reward value. However, this area, along with orbitofrontal cortex, was also required for learning driven by changes in reward identity. This observation requires that existing models of TDRL in the ventral striatum be modified to include information about the specific features of expected outcomes derived from model-based representations, and that the role of orbitofrontal cortex in these models be clearly delineated.
2010
Wilson, R. C., Takahashi, Y. K., Roesch, M. R., Stalnaker, T. A., Schoenbaum, G., & Niv, Y. (2010). A Computational Model of the Role of Orbitofrontal Cortex and Ventral Striatum in Signalling Reward Expectancy in Reinforcement Learning. In Society for Neuroscience Abstracts. PDFAbstract
Both the orbitofrontal cortex (OFC) and ventral striatum (VS) have been implicated in signalling reward expectancies. However, exactly what roles these two disparate structures play, and how they are different is very much an open question. Recent results from the Schoenbaum lab (Takahashi et al., this meeting) describing the detailed effect of OFC lesions on putative reward prediction error signalling by midbrain dopaminergic neurons of rats, point to one possible delineation. Here we describe a reinforcement learning (RL) model of the Takahashi et al. results, that suggests related, but slightly different roles for the OFC and VS in signalling reward expectancies. We present an actor/critic model with one actor (putatively the dorsal striatum) and two critics (OFC and VS). We hypothesise that the VS critic learns state values relatively slowly and in a model free way, while OFC learns state values faster and in a model based way, using one step look ahead. Both areas contribute to a single prediction error signal, computed in ventral tegmental area (VTA), that is used to teach both critics and the actor. As they receive the same teaching signal, the critics, OFC and VS, essentially compete for the value of each state. Our model makes a number of predictions regarding the effects of OFC and VS lesions on the response properties of dopaminergic (putatively prediction error encoding) neurons in VTA. The model predicts that lesions to either VS or OFC result in persistent prediction errors to predictable rewards and diminished prediction errors on the omission of predictable rewards. At the time of a reward predicting cue, the model predicts that these lesions cause both positive and negative prediction errors to be diminished. When the animal is free to choose between a high and low valued option, we predict a difference between the effects of OFC and VS lesions. In the “unlesioned” model, because of the proposed look-ahead abilities of OFC, the model predicts differential signals at the time at which the decision is made, corresponding to whether the high or low valued option has been chosen. When the model-OFC is “lesioned”, however, these differential signals disappear as the model is no longer aware of the decision that will be made. This is not the case when model-VS is “lesioned” in which case the difference between high and low valued options persists. These predictions regarding OFC lesions are born out in Takahashi et al.'s experiments on rats.
Gershman, S. J., Blei, D. M., & Niv, Y. (2010). Context, Learning, and Extinction. Psychological Review , 117 (1), 197–209. PDFAbstract
A. Redish et al. (2007) proposed a reinforcement learning model of context-dependent learning and extinction in conditioning experiments, using the idea of "state classification" to categorize new observations into states. In the current article, the authors propose an interpretation of this idea in terms of normative statistical inference. They focus on renewal and latent inhibition, 2 conditioning paradigms in which contextual manipulations have been studied extensively, and show that online Bayesian inference within a model that assumes an unbounded number of latent causes can characterize a diverse set of behavioral results from such manipulations, some of which pose problems for the model of Redish et al. Moreover, in both paradigms, context dependence is absent in younger animals, or if hippocampal lesions are made prior to training. The authors suggest an explanation in terms of a restricted capacity to infer new causes.
Diuk, C., Botvinick, M. M., Barto, A. G., & Niv, Y. (2010). Hierarchical reinforcement learning: an fmri study of learning in a two-level gambling task. In Neuroscience Meeting Planner.
Todd, M. T., Cohen, J. D., & Niv, Y. (2010). Identifying internal representations of context in fMRI. In Society for Neuroscience Abstracts.
Dayan, P. D., Daw, N. D., & Niv, Y. (2010). Learning, Action, Inference and Neuromodulation. Encyclopedia of Neuroscience (pp. 455–462). PDFAbstract
Neuromodulators such as dopamine, serotonin, norepinephrine, and acetylcholine play a critical role in controlling the learning about the association between stimuli and actions and rewards and punishments, and also in regulating the way that networks process information and effect decisions. Precise characterization of at least one part of their function in these respects comes from theories originating in statistics, operations research, and engineering, and computational theory ties together neural, psychological, ethological, and even economic notions. ©2009 Elsevier Ltd All rights reserved.
Gershman, S. J., & Niv, Y. (2010). Learning latent structure: carving nature at its joints. Curr Opin Neurobiol , 20 (2), 251–256. PDFAbstract
Reinforcement learning (RL) algorithms provide powerful explanations for simple learning and decision-making behaviors and the functions of their underlying neural substrates. Unfortunately, in real-world situations that involve many stimuli and actions, these algorithms learn pitifully slowly, exposing their inferiority in comparison to animal and human learning. Here we suggest that one reason for this discrepancy is that humans and animals take advantage of structure that is inherent in real-world tasks to simplify the learning problem. We survey an emerging literature on 'structure learning'–using experience to infer the structure of a task–and how this can be of service to RL, with an emphasis on structure in perception and action.
Gershman, S. J., Cohen, J. D., & Niv, Y. (2010). Learning to selectively attend. In 32nd Annual Conference of the Cognitive Science Society. PDFAbstract
How is reinforcement learning possible in a high-dimensional world? Without making any assumptions about the struc- ture of the state space, the amount of data required to effec- tively learn a value function grows exponentially with the state space’s dimensionality. However, humans learn to solve high- dimensional problems much more rapidly than would be ex- pected under this scenario. This suggests that humans em- ploy inductive biases to guide (and accelerate) their learning. Here we propose one particular bias—sparsity—that amelio- rates the computational challenges posed by high-dimensional state spaces, and present experimental evidence that humans can exploit sparsity information when it is available.
Niv, Y., & Gershman, S. J. (2010). Representation Learning and Reinforcement Learning : An fMRI study of learning to selectively attend. In Society for Neuroscience Abstracts.