Priming Spatial Activity by Single-Cell Stimulation in the Dentate Gyrus of Freely Moving Rats

An essential requirement for hippocampal circuits to function in episodic memory is the ability to rapidly disambiguate and store incoming sensory information. This "pattern separation" function has been classically associated to the dentate gyrus, where spatial learning is accompanied by rapid and persistent modifications of place-cell representation. How these rapid modifications are implemented at the cellular level has remained largely unresolved. Here, we tested whether plasticity-inducing stimuli--spike trains--evoked in postsynaptic neurons are sufficient for the rapid induction of place-field activity in the dentate gyrus. We juxtacellularly stimulated 67 silent granule cells while rats explored a maze for the first time. Spike trains with different characteristics (e.g., number of spikes, frequency, and theta-rhythmicity) were evoked at randomly selected spatial locations. We found that, under novelty, ∼30% (10/33) of the stimulated neurons fired selectively at the "primed" spatial location on subsequent laps. Induced place fields were either transient or persisted for multiple laps. The "priming" effect was experience dependent, as it was less frequently observed in habituated animals (3/34 neurons), and it correlated with the number of spikes and theta-rhythmicity of the stimulus trains. These data indicate that, albeit with low efficiency, evoked theta-rhythmic spike trains can be sufficient for priming spatial activity in the dentate gyrus and thus recruiting silent granule cells into the coding population.