Informativeness, contingency and time scale invariance in associative learning

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 supports 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.

Methods
Complete Methods are provided in the article: Learning Depends on the Information Conveyed by Temporal Relationships Between Events and is Reflected in the Dopamine Response to Cues. 

Briefly:

Male, Sprague-Dawley rats were housed in groups of two in a colony room on a 12:12 hour light:dark cycle. Water was available ad-lib in the home cages. They were fed in their home cages for one hour after experimental sessions, which occurred 5 days per week. On weekends, they had ad-lib access to food until approximately 22 hours before the first weekday session. They were approximately two months old at the start of training and had been handled for one week before that.  They were trained in eight identical experimental chambers (30.5 cm x 24.1 cm x 21.0 cm) located in ventilated and soundproof boxes. Each chamber was equipped with a speaker, a house light, and a pellet dispenser (Model ENV-203, Med Associates), which delivered 20mg pellets into a head-entry-detecting trough (Models ENV-200R7 and ENV-254-CB, Med Associates). They initially received 2 sessions of magazine training, during which 40 pellets were delivered at random times during a 20-minute session (random time 30s schedule), followed by daily sessions with one of the experimental protocols. The time of occurrence of each head entry and the time of onset and termination of all stimulus events were recorded with 0.1s resolution.