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Abstract

During brain development, before sensory systems become functional,
neuronal networks spontaneously generate repetitive bursts of neuronal
activity, which are typically synchronized across many neurons. Such
activity patterns have been described on the level of networks and
cells, but the fine-structure of inputs received by an individual neuron
during spontaneous network activity has not been studied. Here, we used
calcium imaging to record activity at many synapses of hippocampal
pyramidal neurons simultaneously to establish the activity patterns in
the majority of synapses of an entire cell. Analysis of the
spatiotemporal patterns of synaptic activity revealed a fine-scale
connectivity rule: neighboring synapses (<16 mu m intersynapse distance)
are more likely to be coactive than synapses that are farther away from
each other. Blocking spiking activity or NMDA receptor activation
revealed that the clustering of synaptic inputs required neuronal
activity, demonstrating a role of developmentally expressed spontaneous
activity for connecting neurons with subcellular precision.