Abstract
Sets of spikes emitted sequentially across neurons constitute fundamental pulse packets in neural information processing, including offline memory replay during hippocampal sharp-wave ripples (SWRs). The relative timing of neuronal spikes is fine-tuned in each spike sequence but can vary between different sequences. However, the microcircuitry mechanism that enables such flexible spike sequencing remains unexplored. We recorded the membrane potentials of multiple hippocampal CA1 pyramidal cells in mice and found that the neurons were transiently hyperpolarized prior to SWRs. The pre-SWR hyperpolarizations were spatiotemporally heterogeneous, and larger hyperpolarizations were associated with later spikes during SWRs. Intracellular blockade of Cl−-mediated inhibition reduced pre-SWR hyperpolarizations and advanced spike times. Single-unit recordings also revealed that the pre-SWR firing rates of inhibitory interneurons predicted the SWR-relevant spike times of pyramidal cells. Thus, pre-SWR inhibitory activity determines the sequential spike times of pyramidal cells and diversifies the repertoire of sequence patterns.
Highlights
Sets of spikes emitted sequentially across neurons constitute fundamental pulse packets in neural information processing, including offline memory replay during hippocampal sharpwave ripples (SWRs)
Recording periods ranged from 1 min 53 s to 34 min 57 s, during which a total of 5971 SWRs were recorded in local field potentials (LFPs)
Neither the means nor the standard deviations (SDs) of SWR-relevant spike times were correlated with the distances from the LFP electrode tips to the recorded cells (Supplementary Fig. 2), indicating that spike times were not influenced by cell locations, at least within our recording areas of φ < 800 μm
Summary
Sets of spikes emitted sequentially across neurons constitute fundamental pulse packets in neural information processing, including offline memory replay during hippocampal sharpwave ripples (SWRs). Hippocampal pyramidal cells that are sequentially activated during behavioral exploration are subsequently reactivated as a time-compressed sequence of spikes during SWRs while the animal is resting or sleeping[11]. This internal replay of behavioral experiences has been posited to contribute to memory consolidation, memory recall, and navigational planning[12,13]. We recorded intracellular activity simultaneously from multiple CA1 pyramidal cells to examine the mechanisms underlying flexible sequential activity of CA1 pyramidal cells at the single-cell level and found that preceding GABAergic inhibition dynamically coordinates the spike times of individual pyramidal cells during SWRs
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