Learning depends on the information conveyed by temporal relationships between events and is reflected in the dopamine response to cues.

Abstract

Contemporary theories guiding the search for neural mechanisms of learning and memory assume that associative learning results from the temporal pairing of cues and reinforcers resulting in coincident activation of associated neurons, strengthening their synaptic connection. While enduring, this framework has limitations: Temporal pairing-based models of learning do not fit with many experimental observations and cannot be used to make quantitative predictions about behavior. Here, we present behavioral data that support an alternative, information-theoretic conception: The amount of information that cues provide about the timing of reward delivery predicts behavior. Furthermore, this approach accounts for the rate and depth of both inhibitory and excitatory learning across paradigms and species. We also show that dopamine release in the ventral striatum reflects cue-predicted changes in reinforcement rates consistent with subjects understanding temporal relationships between task events. Our results reshape the conceptual and biological framework for understanding associative learning.