Imaging of spatiotemporal synaptic inputs underlying memory replay

Abstract

Sequential firing is a prominent feature of population activity in exploratory behavior. During the subsequent immobility and sleep period, the sequential firings spontaneously are replayed accompanying high-frequency field oscillations called sharp-wave (SW) ripples. The replays of sequential firing and SWs are considered a key mechanism to achieve normal memory function. However, how a downstream neuron decodes this spatiotemporally organized activity remains unexplored in subcellular resolution. To monitor the calcium activity of dendritic spines from multiple dendritic trees of a neuron in an ex vivo network, we established a new optical recording technique for functional multiple-spine calcium imaging (fMsCI). Using fMsCI, we discovered that neurons that fired spikes frequently in SWs received increasing synaptic inputs during SWs. The synaptic barrages during SWs were composed of a rich repertoire of sequential structures on nearby synapses. Our data suggest that sequential spikes of hippocampal memory engrams may excite neighboring spines of a postsynaptic neuron in a different order, which may partially explain the specific activation of SW participants during SWs.