CA1 ensemble plasticity is coupled to context change and modulated by task familiarity

ABSTRACT When should plasticity mechanisms get recruited (stability-plasticity dilemma)? Environments change over time, re/entering a given context increases uncertainty and predicts the need for updating. Hippocampus (HPC) is key to tracking context change but also navigation in relation to moving targets. CA1 ensembles expressing immediate-early genes (IEGs) are contextually specific, while the amount of IEG expression correlates with HPC-dependent task demands. However, task effects on the IEG-expressing ensembles per se remain unclear. In three experiments, we tested the effect of context change and HPC task demands on CA1 IEG+ ensembles in rats. Experiment 1 showed that the IEG+ ( Arc , Homer1a RNA) ensemble size drops to baseline level during uninterrupted 30 min exploration, reflecting familiarization and decreasing uncertainty, unless context change is present; the ensemble sizes reflect both context identity and context change. Experiment 2 showed no evidence of task-specificity of IEG+ ensembles during highly HPC-dependent mobile robot avoidance nor HPC-independent stationary robot avoidance. Experiment 3 replicated the findings of Experiment 2 for c-Fos protein. Nonetheless, the data suggest that ensembles shrink with task mastery/familiarity and grow with novelty presented by acquisition of behavioral extinction. Overall, our results shed light on the temporal dynamics, and the context and task control of CA1 IEG+ ensembles. The present results and the relevant literature suggest that context change resets the ensemble of IEG-expressing CA1 neurons and novelty delays the time-dependent ensemble shrinking. HIGHLIGHTS Plasticity and learning rate should reflect novelty and familiarity, i.e. uncertainty Change of context and task requirements increase uncertainty Familiarization with context and task reduces uncertainty For context, this pattern is matched by dynamics of IEG+ ensembles in CA1 Task demands have modulating influence on CA1 IEG+ ensembles GRAPHICAL ABSTRACT