Distinct spatial distribution of potentiated dendritic spines in encoding- and recall-activated hippocampal neurons

Experimental advancements in neuroscience have identified cellular engrams—ensembles of neurons whose activation is necessary and sufficient for memory retrieval. Synaptic plasticity, including long-term potentiation, is fundamental to memory encoding and recall, but the relationship between learning-induced dendritic spine potentiation and neuron-wide activation remains unclear. In this study, we employed a post-synaptic translation-dependent reporter consistent with potentiation (SA-PSDΔVenus) and a neuronal activation reporter (ESARE-dTurquoise) to determine their spatiotemporal correlation in the mouse hippocampal CA1 following contextual fear conditioning (CFC). SA-PSDΔVenus+ spines were enriched in ESARE-dTurquoise+ neurons, with distribution varying across CA1 layers at different phases of memory: SA-PSDΔVenus+ were more frequent in activated neurons in stratum oriens and stratum lacunosum moleculare after CFC (encoding), while recall-activated neurons showed a larger number of SA-PSDΔVenus+ in the stratum radiatum . These findings demonstrate that the relative weight and spatial distribution of potentiated synaptic inputs to hippocampal CA1 pyramidal neurons change between the encoding and retrieval phases of memory.