Enrichment experience improves hippocampal sparse coding via inhibitory circuit plasticity

Abstract

Environmental enrichment enhances hippocampus-dependent learning and memory, yet the underlying circuit mechanisms remain largely unknown. Here we combined miniscope calcium imaging during spatial exploration with synaptic circuit analysis in hippocampal slices to determine how enrichment experience alters hippocampal network dynamics. Prolonged enrichment reduced average firing rates and immediate early gene expression in CA1 pyramidal cells, while increasing peak firing and spatial selectivity. Population activity was sparser and more diverse, resulting in a higher Gini index. Circuit analysis revealed enhanced excitatory drive onto both pyramidal cells and somatostatin (SOM) interneurons, together with a strengthened SOM-mediated feedback inhibition onto pyramidal cells. Suppressing SOM interneurons occluded the enrichment-induced augmentation of sparsity and Gini index and prevented improvements in hippocampus-dependent learning. These findings demonstrate that environmental enrichment dynamically enhances hippocampal sparse coding through potentiation of SOM-mediated feedback inhibition, linking experience-dependent inhibitory plasticity to enhanced memory performance.