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Local generation of multineuronal spike sequences in the hippocampal CA1 region

Significance Neuronal sequences in the CA1 hippocampal region during short burst events (called sharp wave ripples) reliably reflect the slower sequential order of place activation during exploration, patterned by local-circuit interneurons. We tested the hypothesis that in addition to afferent drive, local mechanisms contribute critically to the sequential patterning of pyramidal cells and the diverse interneuron types. We show that optogenetic activation of a small group of CA1 pyramidal cells in mouse hippocampus yields consistent multineuronal spike sequences, and that their sequential firing order is similar to that observed during spontaneous “ripple” and theta oscillations. Thus, multineuronal spike sequences are not exclusively inherited from upstream sources but result from local-circuit dynamics and biophysical properties of the individual neurons. Sequential activity of multineuronal spiking can be observed during theta and high-frequency ripple oscillations in the hippocampal CA1 region and is linked to experience, but the mechanisms underlying such sequences are unknown. We compared multineuronal spiking during theta oscillations, spontaneous ripples, and focal optically induced high-frequency oscillations (“synthetic” ripples) in freely moving mice. Firing rates and rate modulations of individual neurons, and multineuronal sequences of pyramidal cell and interneuron spiking, were correlated during theta oscillations, spontaneous ripples, and synthetic ripples. Interneuron spiking was crucial for sequence consistency. These results suggest that participation of single neurons and their sequential order in population events are not strictly determined by extrinsic inputs but also influenced by local-circuit properties, including synapses between local neurons and single-neuron biophysics.