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.