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. HIGHLIGHTSO_LIPlasticity and learning rate should reflect novelty and familiarity, i.e. uncertainty C_LIO_LIChange of context and task requirements increase uncertainty C_LIO_LIFamiliarization with context and task reduces uncertainty C_LIO_LIFor context, this pattern is matched by dynamics of IEG+ ensembles in CA1 C_LIO_LITask demands have modulating influence on CA1 IEG+ ensembles C_LI GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=140 SRC="FIGDIR/small/608588v1_ufig1.gif" ALT="Figure 1"> View larger version (26K): org.highwire.dtl.DTLVardef@12808c0org.highwire.dtl.DTLVardef@156ad3corg.highwire.dtl.DTLVardef@1876f0aorg.highwire.dtl.DTLVardef@8b13f4_HPS_FORMAT_FIGEXP M_FIG C_FIG