Benefitting from trial spacing without the cost of prolonged training: Frequency, not duration, of trials with absent stimuli enhances learning

The statistical relation between two events influences the perception of how well one event relates to the presence or absence of another. The simultaneous absence of both events, just like their mutual occurrence, is theoretically relevant for describing their contingency. However, humans tend to weight co-occurring information more heavily than co-absent information. We explored the relevance of co-absent events by varying the duration and frequency of trials without stimuli. In three experiments, we used a rapid trial streaming procedure, and found that the perceived association between events is enhanced with increased frequency of co-absent events. Duration of co-absent events did not play as strong role on judgments of association as did frequency. These findings suggest ways in which the benefits of trial spacing, which are effectively co-absence events, could be preserved without increasing total training time. Specifically, the present results suggest that the benefits of distributed practice can be obtained without increasing the length of the training session by shortening the intervals between events. We also discuss five potential accounts of how the co-absent experience is processed: contingency sensitivity, a memory testing effect, associative interference, reduced cognitive load, and consolidation.

Spaced training enhances memory and prefrontal ensemble stability in mice

SummaryMemory is substantially improved when learning is distributed over time, an effect called “spacing effect”. So far it has not been studied how spaced learning affects neuronal ensembles presumably underlying memory. In the present study, we investigate whether trial spacing increases the stability or size of neuronal ensembles. Mice were trained in the “everyday memory” task, an appetitive, naturalistic, delayed matching-to-place task. Spacing trials by 60 minutes produced more robust memories than training with shorter or longer intervals. c-Fos labeling and chemogenetic inactivation established the necessity of the dorsomedial prefrontal cortex (dmPFC) for successful memory storage. In vivo calcium imaging of excitatory dmPFC neurons revealed that longer trial spacing increased the similarity of the population activity pattern on subsequent encoding trials and upon retrieval. Conversely, trial spacing did not affect the size of the total neuronal ensemble or the size of subpopulations dedicated to specific task-related behaviors and events. Thus, spaced learning promotes reactivation of prefrontal neuronal ensembles processing episodic-like memories.

Associative Learning from Replayed Experience

We develop an extension of the Rescorla-Wagner model of associative learning. In addition to learning from the current trial, the new model supposes that animals store and replay previous trials, learning from the replayed trials using the same learning rule. This simple idea provides a unified explanation for diverse phenomena that have proved challenging to earlier associative models, including spontaneous recovery, latent inhibition, retrospective revaluation, and trial spacing effects. For example, spontaneous recovery is explained by supposing that the animal replays its previous trials during the interval between extinction and test. These include earlier acquisition trials as well as recent extinction trials, and thus there is a gradual re-acquisition of the conditioned response. We present simulation results for the simplest version of this replay idea, where the trial memory is assumed empty at the beginning of an experiment, all experienced trials are stored and none removed, and sampling from the memory is performed at random. Even this minimal replay model is able to explain the challenging phenomena, illustrating the explanatory power of an associative model enhanced by learning from remembered as well as real experiences.