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A key question in decision-making is how humans arbitrate between competing learning and memory systems to maximize reward. We address this question by probing the balance between the effects, on choice, of incremental trial-and-error learning versus episodic memories of individual events. Although a rich literature has studied incremental learning in isolation, the role of episodic memory in decision-making has only recently drawn focus, and little research disentangles their separate contributions. We hypothesized that the brain arbitrates rationally between these two systems, relying on each in circumstances to which it is most suited, as indicated by uncertainty. We tested this hypothesis by directly contrasting contributions of episodic and incremental influence to decisions, while manipulating the relative uncertainty of incremental learning using a well-established manipulation of reward volatility. Across two large, independent samples of young adults, participants traded these influences off rationally, depending more on episodic information when incremental summaries were more uncertain. These results support the proposal that the brain optimizes the balance between different forms of learning and memory according to their relative uncertainties and elucidate the circumstances under which episodic memory informs decisions. 

Abstract Previous research has stressed the importance of uncertainty for controlling the speed of learning, and how such control depends on the learner inferring the noise properties of the environment, especially volatility: the speed of change. However, learning rates are jointly determined by the comparison between volatility and a second factor, moment-to-moment stochasticity. Yet much previous research has focused on simplified cases corresponding to estimation of either factor alone. Here, we introduce a learning model, in which both factors are learned simultaneously from experience, and use the model to simulate human and animal data across many seemingly disparate neuroscientific and behavioral phenomena. By considering the full problem of joint estimation, we highlight a set of previously unappreciated issues, arising from the mutual interdependence of inference about volatility and stochasticity. This interdependence complicates and enriches the interpretation of previous results, such as pathological learning in individuals with anxiety and following amygdala damage. 

Abstract It is thought that the brain’s judicious reuse of previous computation underlies our ability to plan flexibly, but also that inappropriate reuse gives rise to inflexibilities like habits and compulsion. Yet we lack a complete, realistic account of either. Building on control engineering, here we introduce a model for decision making in the brain that reuses a temporally abstracted map of future events to enable biologically-realistic, flexible choice at the expense of specific, quantifiable biases. It replaces the classic nonlinear, model-based optimization with a linear approximation that softly maximizes around (and is weakly biased toward) a default policy. This solution demonstrates connections between seemingly disparate phenomena across behavioral neuroscience, notably flexible replanning with biases and cognitive control. It also provides insight into how the brain can represent maps of long-distance contingencies stably and componentially, as in entorhinal response fields, and exploit them to guide choice even under changing goals. 

To make effective decisions, people need to consider the relationship between actions and outcomes. These are often separated by time and space. The neural mechanisms by which disjoint actions and outcomes are linked remain unknown. One promising hypothesis involves neural replay of nonlocal experience. Using a task that segregates direct from indirect value learning, combined with magnetoencephalography, we examined the role of neural replay in human nonlocal learning. After receipt of a reward, we found significant backward replay of nonlocal experience, with a 160-millisecond state-to-state time lag, which was linked to efficient learning of action values. Backward replay and behavioral evidence of nonlocal learning were more pronounced for experiences of greater benefit for future behavior. These findings support nonlocal replay as a neural mechanism for solving complex credit assignment problems during learning.