Abstract
Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep. Neurons active during behavior reactivate in both structures during sleep, in conjunction with characteristic brain oscillations that may form the neural substrate of memory consolidation. In the hippocampus, replay occurs within sharp wave-ripples: short bouts of high-frequency activity in area CA1 caused by excitatory activation from area CA3. In this work, we develop a computational model of ripple generation, motivated by in vivo rat data showing that ripples have a broad frequency distribution, exponential inter-arrival times and yet highly non-variable durations. Our study predicts that ripples are not persistent oscillations but result from a transient network behavior, induced by input from CA3, in which the high frequency synchronous firing of perisomatic interneurons does not depend on the time scale of synaptic inhibition. We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration. Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network.
Highlights
Sleep, which consumes about a third of our lives, is thought to play a critical role in memory consolidation
We develop a computational model of ripple generation, motivated by in vivo rat data showing that ripples have a broad frequency distribution, exponential interarrival times and yet highly non-variable durations
We propose a novel mechanism of ripple generation consistent with a wide range of experimental data, to explain how hippocampal network properties shape ripple frequency and duration
Summary
Sleep, which consumes about a third of our lives, is thought to play a critical role in memory consolidation. The hippocampus generates sharp wave-ripple complexes (SWR), in which a strong excitatory input from CA3 pyramidal cells leads to broadly distributed postsynaptic potentials (the sharp waves) in CA1 stratum radiatum, while the pyramidal layer shows a quick bout of high frequency LFP activity (the ripple) [9–11]. Ripples exist both in a quiet awake state and during slow-wave sleep, and disruption of ripple activity is known to impair memory [12, 13]
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